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THE VERTEBRATE EYE

AND ITS ADAPTIVE RADIATION

GORDON LYNN WALLS

Research Associate in Ophthalmology,
Wayne University College of Medicine

HAFNER PUBLISHING COMPANY

New York London

1963

reprinted by arrangement with
The Cranbrook Institute of Science

Printed and Published by

Hafner Publishing Company

31 East 10th Street

New York 3, New York

Library of Congress Catalog Card Number 63-17545

(§) copyright 1942

The Cranbrook Institute of Science

Bloomfield Hills, Michigan

All rights reserved. This book, or parts thereof, may
not be published in any form without the written
permission of the publishers.

PREFACE

The stmctural patterns of vertebrate eyes have been undergoing
intelligent scrutiny for about a century and a half. In that time, and
more and more rapidly toward the present, men have been learning
much about the functional meanings of those patterns, and their roles
in the lives of the animals which have produced them. It has seemed
to me that it is time an attempt was made to interpret comparative
ocular biology as a whole to those who want to know what the eye is
all about, but are repelled by the pedantic terminology of anatomy
texts, the mathematics of physiological optics, the scatteredness of the
ecological literature, and the German language. In this book, I have
made such an attempt.

I have chosen the term 'adaptive radiation' for the subtitle of this
work deliberately. It was coined by Henry Fairfield Osborn to describe
the manner in which animal groups have become diversified in pouring
themselves into a number of environmental molds which were made
available to them more or less simultaneously. It is a little unusual to
speak of the adaptive radiation of an organ; but I can think of no
better way to express what the vertebrate eye has done in modifying its
pattern to fit itself for the many different kinds of performance de-
manded of it by its adaptively-radiated owners.

The investigation of anatomy for its own sake is pretty well defunct.
The study of structures in relation to their employment by the animal
has hardly begun. When I started writing this book, I had never heard
of the late Hans Boker; but, in discussing the eyes of vertebrates in
terms of adaptation to environment, I believe I have followed the prin-
ciples of his 'comparative biological anatomy', which have so revivified
the study of anatomy in recent years.

If the comparative ophthalmologists of the world should ever hold
a convention, the first resolution they would pass would say: "Every-
thing in the vertebrate eye means something." Except for the brain,
there is no other organ in the body of which that can be said. It does
not matter in the least whether a liver has three lobes or four, or
whether the tip of the heart points north or south, or whether a hand
has five fingers or six, or whether a kidney is long and narrow or short
and wide. But if we should make comparable changes in the makeup of

PREFACE

a vertebrate eye, we should quite destroy its usefulness. Man can make
optical instruments only from such materials as brass and glass. Nature
has succeeded with only such things as leather and water and jelly; but
the resulting instrument is so delicately balanced that it will tolerate no
tampering.

And yet, vertebrate eyes are not all alike — far from it. Each is a
cluster of harmonious parts, and the changes which have converted one
type of eye into another, through evolution, have necessarily involved
most of its parts. When one feature has had to be altered for some
primary ecological reason, this alteration has in turn called for con-
current secondary alterations of other structures, with the whole complex
remaining harmonious and workable at all times. Of course, many eyes
contain little odds and ends of structures which have no function. But
in every such case, one can be sure that the structure in question did not
arise in its present form, but is a vestige of a once important part which
is no longer needed, or whose task has come to be done better by some-
thing else in the eye. When such remnants are in the way — and they
usually are — the eye gets rid of them promptly, which may add greatly
to the difficulty of determining how the ocular pattern of a given group
was ever derived from that of a known ancestor. Fortunately, however,
there are few such gaps; and it is now possible to tell a well-connected
story of the evolution of almost any particular vertebrate eye.

This book will be of particular benefit to zoologists and ecologists,
medical and veterinary ophthalmologists, and comparative psychologists.
But since none of these people speak the others' languages, I have been
able to assume no more scientific knowledge on the reader's part than the
contents of the usual elementary course in biology. The book should
therefore be entirely clear to any college student or graduate, and to any
amateur naturalist — 'trained' or not. As each unusual term has been
introduced, I have either defined it there and then or else placed it in the
glossary. The reader will find that the difficulty of the reading fluctuates,
which is inevitable in view of the varying weightiness of the material.
Some things about the eye and its workings are intricate, but I must
disclaim all responsibility for that — there are some subjects, such as
astrophysics and thermodynamics, which no writer could possibly 'pop-
ularize'. The reader will also soon note that my mode of expression is
strongly tainted with teleology. I do not expect this to mislead anyone —
it is merely an economy device, for it saves many words to say simply that
an animal has produced this feature or that to fill such-and-such a need.

PREFACE

The material of the book is progressive, though this may not seem
to be indicated by the table of contents. I could not explain everything
at once, but I have so arranged matters that a given discussion will be
perfectly lucid if the reader has not skipped much before it. I hope,
naively of course, that anyone who reads in the book at all will read
the whole of it. It is not designed as a reference book, in which to
'look up' small points from time to time. Rather, it has been written
in the style of a text-book, though for a course which has yet to be
given in any American university. The book is not documented, i.e.
loaded up with specific citations for every point of fact and reasoning
which has originated outside of my own studies. The average reader
will not miss them; and the earnest student who reads the book, and
is led thereby to want to do research in its field, will have to devour all
of the required reading listed in the bibliography anyway. He — and
the established investigator in the field — will readily know which of my
pronouncements to blame upon me alone. If not, he is free to write to
me for specific bibliographic assistance, which I shall gladly furnish
within the limitations of my time and ability.

Part I has been called 'basic' because it incorporates the first bodies
of information which the reader should have if he knows little or nothing
about the eye to begin with — even if he intends to skip straight to
Chapter 17 to find out what the pecten means. It is strongly urged that
every reader, even the ophthalmologist, read all of Part I before attempt-
ing to appreciate other chapters. In it, the human eye and human vision
have been used to acquaint the reader thoroughly with one sample eye
and its workings. The all-important retina is discussed in general terms.
The origins of the eye, ontogenetic and phylogenetic, are explained; and
the elementary facts of vertebrate inter-relationships are set forth so that
the non-zoological reader will understand the necessary taxonomic allu-
sions in Part II and the discussions of relationships and derivations
in Part III.

Part II is the ecological body of the work. Here are gathered to-
gether, unoier the banners of various environmental factors, the evolu-
tionary responses of the vertebrate eye to those factors. In these chapters,
at some risk of cluttering, I have included many cross-references to
ensure that the reader who insists on dabbling will not miss information
pertinent to the satisfaction of his momentary curiosity. Some matters
are expounded in more detail than others, somewhat in proportion to
the interest I have found them to arouse — the subject of animal color

PREFACE

vision, for example, is treated at particular length because no questions
are so often asked of the comparative ophthalmologist as those under
this aegis. Part II is an exposition of fundamental ideas rather than a
compendium of both explicable and at-present-useless facts. Because of
its ecological viewpoint, whole great fields find no place in it (or else-
where in this book) — ocular biochemistry, retinal photo-electrics, clinical
veterinary ophthalmology, most of physiological optics, and so on.
These chapters are intended to stimulate as well as to inform, and both
here and in Part III there is emphasis upon the more conspicuous of the
unsolved problems which await new students.

Part III traces the history of the eye, group by group, from the lowest
living vertebrates to the highest. Here, place has been made for those
features which are of importance to the eye itself as a living thing, but
are not discemibly concerned in its performance in relation to the special
environment of its owner. The emphasis in these synoptic chapters is on
the morphology of the eye, the evolution of that morphology, and the
bearing of it upon the problems of vertebrate phylogeny. The animal as
a whole explains much about its eye, and in turn the eye can often
explain much about the animal. Thus, the structural plan of the snake
eye, its possible mode of origin, and the significance of this for the
evolutionary history of the snakes, are all interconnected matters. The
reader will find numerous sub-indices in Part III which will enable him
to round up quickly all the information about his favorite group which
has been given earlier in the book, and is omitted here to avoid dupli-
cation and waste of space.

The illustrations have been kept as simple as possible, considering the
intricacies of the subject. Many are original, several of them — quite be-
yond my ability to make — beautifully drawn by the Misses Sylvia Hag-
yard and Gladys Larsen. Many others have been borrowed photograph-
ically from the journals, with or without changes (which are noted in
the legends) , and relabelled in accordance with a uniform scheme. Here,
much of the burden of work fell upon Albert Schlorff, without whose
expert photographic assistance I should have been quite helpless. I must
also acknowledge with gratitude the kindness of Viktor Franz in per-
mitting the free use of illustrations from his work. Figures 4, 5, and 41d
are by courtesy of William Bloom and the W. B. Saunders Company,
publishers of his 'Maximow's Text-Book of Histology'. Figures 6a and
16 are modified from Adler's 'Clinical Physiology of the Eye', by per-
mission of The MacMillan Company, publishers.

PREFACE

A great number of my friends have helped materially to make this
book possible, by criticizing portions of the manuscript relating to their
specialties, by furnishing specimens, information, or technical assistance;
and in other ways. I could not omit to mention some of them by name :
Ermine C. Case, Alfred Cowan, Elizabeth Crosby, Brian Curtis, Walter
F. Grether, Parker Heath, Selig Hecht, Arlington C. Krause, George
E. Lathrop, Wade H, Marshall, George A. Moore, Kevin J. O'Day,
Erich Sachs, John F. Shepard, Alec Skolnick, Gabriel Steiner, Francis
B. Sumner, Samuel A. Talbot, and Burton D, Thuma. During the
writing, generous financial support was forthcoming from the Wayne
University College of Medicine and from the Jennie Grogan Mendelson
Memorial Fund for Ophthalmology. During the actual making of the
book, the expert and sympathetic guidance of William L. Wood,
director of the Cranbrook Press, has been invaluable.

I am particularly obligated to the curators of the Museum of Zoology
of the University of Michigan and the Cranbrook Institute of Science
who read the entire text and straightened my kinks in their especial
realms: Carl L. Hubbs (fishes), Helen T, Gaige (amphibians and
reptiles) , Josselyn Van Tyne (birds) , and Robert T, Hatt (mammals) .

Finally, I am most deeply indebted of all to Director Hatt and the
Trustees of the Institute for their invitation to write the book as one of
their series of Bulletins, and for their generosity in the allowance of
space and illustrations. As is so usual with such books, the problem has
been to know how much to leave out. My trepidations in this connection
have led, during the writing, to several upward revisions of the expected
size of the work. I have felt as though I were behaving rather like the
camel which at first asked only to warm his nose within the Arab's tent,
and finished by crowding out the owner. My conscience will be easier
if most of my readers are glad that the book was not smaller.

G. L. W.
Detroit, Michigan
May, 1942

TABLE OF CONTENTS
Part I— Basic

Chapter Page

1. LIGHT AND ITS PERCEPTION 1

2. A TYPICAL VERTEBRATE EYE: THE HUMAN 6

A. Structures and their Functions 6

The Eye a 'Camera', 6 — The Fibrous Tunic, 7 — The Intra-
Ocular Fluids, 12— The Uveal Tract, 13— The Pupil, 17

— The Lens and Zonule, 19.

B. Optics and Accommodation 22

Refraction, 22 — Action of a Convex Lens, 2^ — Refractive
Errors of the Eye, 26 — Dioptrics of the Normal Eye, 29 —
Accommodation, 30.

C. The Ocular Adnexa 36

The Oculomotor Muscles, 36— The Lids, 38 — The Lac-
rimal System, 41.

3. THE VERTEBRATE RETINA 42

A. Histology and Physiology 42

The Pigment Epithelium, 42 — The Visual-Cell Layer, 45

— The Bipolar Layer, 46 — The Ganglion Layer, 47 —
Miiller Fibers, 48 — Neuroglia, 48 — Horizontal and Ama-
crine Cells, 49 — Nutrition of the Retina, 50 — The Optic
Nerve, 51.

B. Types of Visual Cells 52

General Types — Rods versus Cones, 52 — Single Cones, 53
— Rods, 57 — Homology of Rods and Cones, 57 — Green
Rods, 58— Double Cones, 58 — Twin Cones, 60 — Ophidian
Double Cones, 61 — Double Rods, 62.

C. The Duplicity Theory 64

History, 64 — Sensitivity versus Acuity, 65 — Retinal Fac-
tors in Acuity, 65 — Retinal Factors in Sensitivity, 68 —
Evidence for Duplicity of Vision, 71.

4. THE VISUAL PROCESS 74

A. ScoTOPic Vision 74

Rhodopsin, 74 — Dark Adaptation, 76 — Rod Vision, 79.

TABLE OF CONTENTS

B. Photopic Vision 81

Cone Vision, 81 — Color, 81 — Saturation, 84 — Brightness
and the Purkinje Phenomenon, 87 — Trichromatic Vision,
88 — Central Events in Trichromatic Vision, 91 — Color
Blindness, 96 — Photochemistry of Color Vision, 100.

5. THE GENESIS OF THE VERTEBRATE EYE . . .104

A. Embryological 104

Formation of the Optic Cup, 104 — Differentiation of the
Retina, 108— The Lens, 109— The Hyaloid Circulation,

113 — The Vitreous, 113 — The Vascular and Fibrous
Tunics, 114 — Lids and Glands, 117 — -Variations in Non-
Mammals, 117.

B. Evolutionary 119

The Eye a 'Part of the Brain', 119 — Early Theories, 120 —
Balfour's Theory, 122 — The Placode Theory, 125 — Bo-
veri's Theory, 125 — Studnicka's Theory, 126 — Origin of
the Retina, 128— Origin of the Lens, 129.

6. ELEMENTS OF VERTEBRATE PHYLOGENY . . .134

Part II — Ecologic

Chapter ^ Page

7. ADAPTATIONS TO ARHYTHMIC ACTIVITY . . 143

A. The Twenty-Four-Hour Habit and the Eye . . 143

B. Retinal Photomechanical Changes . . .145

Pigment Migration, 146 — ^Visual-Cell Movements, 147 —
Significance and Distribution, 149 — Immediate Causation,
151.

C. Pupil Mobility 153

Functions of the Pupil, 153 — Pupillary versus Retinal
Adaptation, 154 — Comparative Survey of the Two Meth-
ods, 158.

D. DuPLiaTY and Transmutation 163

8. ADAPTATIONS TO DIURNAL ACTIVITY .169

A. DiuRNALiTY AND THE Eye 169

Diumality and Sharp Vision, 169 — Diurnality, Acuity,

and Food, 169— The Eye as a Whole, 171.

B. The Diurnal Retina 175

Cone: Rod and Receptor: Conductor Ratios, 175 — Minimiz-
ation of the Physiological Scotoma, 178.

TABLE OF CONTENTS

C. Are^ Centrales and Foveje 181

The Area Centralis, 181 — The Fovea, 182 — Distribution,
184.

D. Intra-Ocular Color-Filters 191

Types and Distribution, 191 — The Color- Vision Theory,

192 — Yellow Filters and Chromatic Aberration, 193 —
Other Values, 195— Red Filters and the Rayleigh Effect,
197— Value of Red Oil-Droplets in Birds, 197— Value of
Red Oil-Droplets in Turtles, 197 — Phylogeny and Chem-
istry of the Intra-Ocular Filters, 199.

9. ADAPTATIONS TO NOCTURNAL ACTIVITY . . 206

A. Nocturnality and the Eye 206

Noctumality and Crude Vision, 206 — Advantages and
Limitations, 208 — Lightless Habitats and their Conquest,

209— Tne Eye as a Whole, 210— Tubular' Eyes, 212—
Spherical Lenses, 213 — Broad Comeae, 214.

B. The Nocturnal Retina 215

Rod: Cone Ratios, 215 — Pure- Rod Animals, 216 — Sum-
mation, 216.

C. The Slit Pupil 217

Value of the Slit Form, 218 — -Distribution and Meanings
of Pupil Shapes, 219.

D. The Tapetum Lucidum 228

Value and Basis of Eyeshine, 229 — The Tapetum Fibro-

sum, 231 — The Tapetum Cellulosum, 233 — Guanin and
the Argentea, 235 — Guanin in Retinal Tapeta, 236 — Other
Retinal Tapeta, 238 — Guanin in Chorioidal Tapeta, 238 —
Phylogeny and Relative Efficiency of Tapeta, 243— The
Tapetum and Visual Acuity, 245.

10. ADAPTATIONS TO SPACE AND MOTION . . .247
A. Accommodation and its Substitutes .... 247
Dependence of Apparent Distance upon Size, 247 — The
Why of Accommodation, 249— Devices Which Make
Accommodation Unnecessary, 253 — Vertebrate Methods
of Accommodation, 257 — Lampreys, 258 — Elasmobranchs,
260— Teleosts, 260--Other Fishes, 263— Matthiessen's
Ratio, 2&\ — Optical Elimination of the Cornea, 2M — Con-
sequences of Lens Movement, 265 — Amphibians, 265 —
Role of the Vitreous in Ichthyopsidan Accommodation, 268
— Sauropsidan Muscles of Accommodation, 269 — Scleral
Ossicles in Sauropsida, 270 — Accommodation in Saurop-
sida (Except Snakes), 275 — Special Features in Birds and
Lizards, 279— Snakes, 282— Mammals, 283.

TABLE OF CONTENTS

B. Visual Angles and Fields 288

Visual Angles, 289 — Position of the Eyes in the Head,
290 — Extent of the Binocular Field, 291 — Devices for
Enlarging the Binocular Field, 299.

C. Eye Movements and the Fovea 300

Kinds of Eye Movements, 300 — Fishes, 303 — Amphibians,
305— Reptiles, 305— Birds, and the Visual Trident, 307—
Mammals, 310.

D. Depth- and Solidity-Perception 313

Clues to Depth and Distance, 313 — Stereopsis in Man,

315 — The Optic Chiasma in Man and Other Vertebrates,
319 — Supposed Value of Partial Decussation, 320 — The
Case for Singleness in Animals, 323 — The Evolution of
Binocular Vision, 326 — The Nature and Basis of Fusion,
331 — The Strange Fate of the Median Eyes, 338 — Sub-
stitutes for Binocular Stereopsis, 341.

E. Movement-Perception 342

Detection versus Saliency, 343 — Grades of Movement, 345
— The Relativity of Movement-Perception, 347 — Motor
Factors in Movement-Detection, 348 — Sensory Factors in
Movement-Detection, 349 — Adaptation, and Center versus
Periphery, 352 — Stroboscopic Movement versus Real Move-
ment, 356 — Stroboscopic Vision in Animals, 362 — Men-
ner's Theory of the Pecten, 365 — Multiple Optic Pap-
illa, 367.

11. ADAPTATIONS TO MEDIA AND SUBSTRATES . . 368

A. Aquatic Vision 368

Definition, 368 — Effect of Water upon the Plan of the

Eye, 369 — Origin of Intra-Ocular Fluids, 371 — Effects of
Water upon Light, 373 — Looking Through the Surface,
377 — Streamlining of the Eyeball, 379 — 'Adipose Lids',
381— Bottom Fishes, 384 — Cave Fishes, 387— Parasitic
Fishes, 390 — Deep-Sea Fishes, 391 — Deep-Sea Larval Eyes,
403 — The Common Eel, 405 — Aquatic Amphibia, 407 —
Sirenians^CC^Whales, 410— Adaptation to Water Pres-
sure?, 415.

B. Aerial Vision 417

Changes in Dioptrics, 417— New Extra-Ocular Structures,
418 — Adnexa in Amphibia, 418 — The Third Lid and the
Fate of the Retractor, 419 — Adnexa in Sphenodon, 420 —
Crocodilians, 421 — Turtles, 422 — Lizards, 423 — Snakes,
424 — Birds, 424 — Mammals, 425 — Inter-Relations of
Globe and Adnexa, 427 — Peculiar Status of the Elasmo-
branchs, 428.

TABLE OF CONTENTS

C. AiR-AND- Water Vision 429

The Main Problem, 429 — Amphibious Vision in Teleosts,

431 — Amphibians and Crocodilians, 436 — Turtles, 436 —
Amphibious Squamates, 438 — Amphibious Birds, 438 —
Amphibious Mammals, 442.

D. The Spectacle 449

Injurious Substrates, 449 — Types of Spectacles, 449 — Pri-
mary Spectacles and the History of the Cornea and Con-
junctiva, 449 — Secondary Spectacles, 453 — Tertiary Spec-
tacles in Reptiles, 454 — Tertiary Spectacles in Fishes, 459.

12. ADAPTATIONS TO PHOTIC QUALITY . . . .462

A. Color Vision in Animals 462

The Limits of the Spectrum, 462 — Value and Origin of

Color Vision — 462 — Evidence for Color Vision, 465 — A
Sample Ideal Procedure for Investigation, 467 — Fishes,
472— Amphibians, 490— Reptiles, 494— Birds, 497— Mam-
mals, 504 — Phylogeny of Color Vision, 518 — Locus of
Color Vision, 521.

B. Dermal Color-Changes 523

Modes of Color Change, 524 — 'Physiological' and 'Morph-
ological' Chromatophoral Changes, 526 — Control Through
the Eye, 527^ — Physiological Color Changes in Teleosts,
528 — Mode of Control in Teleosts, 529 — Response to
Albedo, 530 — Morphological Color Changes in Teleosts,
532 — Color Changes in Amphibians, 535 — Dermal Changes
in Lower Fishes, and 'Diurnal Rhythms', 537 — Color
Changes in Reptiles, 538.

C. Coloration of the Eye 543

Basis of Iris Colors, 543— Possible Significance, 543 —
Conspicuousness of the Eye, 544 — Concealment of the
Eye?, 544 — Concealment of the Pupil?, 548— Sexual and
Temporal Differences, 549.

Part III — Synoptic

Chapter ^ ^ Page

13. CYCLOSTOMES 555

A. Lampreys 555

The Eye as a Whole, 555— The Retina, 560.

B. Hags 562

14. HIGHER FISHES 563

A. Elasmobranchs 563

The Eye as a Whole, 563— The Retina, 568.

TABLE OF CONTENTS

B. Chondrosteans 569

The Eye as a Whole, 569— The Retina, 572.

C HOLOSTEANS AND TeLEOSTS 573

Holosteans, 573 — The Holostean Retina, 576 — Teleosts,
576— The Teleost Retina, 584.
D. Cladistians and Dipnoans . . . . . . 588

Cladistians, 589 — Dipnoans, 589 — The Dipnoan Retina,
590.

15. AMPHIBIANS 592

A. Anurans 593

The Eye as a Whole, 593— The Retina, 598.

B. Urodeles 600

The Eye as a Whole, 601 — The Retina, 603 — Comparison
with Fishes, 604.

C. C^CILIANS 605

16. REPTILES *..... 607

A. Chelonians 608

The Eye as a Whole, 609— The Retina, 611.

B. Crocodilians 613

The Eye as a Whole, 613— The Retina, 615.

C. Sphenodon 616

The Eye as a Whole, 617— The Retina, 620.

D. Squamates 622

Lizards, 622 — The Lacertilian Retina, 625— Snakes, 627 — ■

The History of the Snake Eye, 632 — The Ophidian Ret-
ina, 636.

17. BIRDS 641

The Eye as a Whole, 641 — The Pecten, and its Analogues
in Other Vertebrates, 648— The Retina, 659.

18. MAMMALS 663

A. Monotremes and Marsupials 664

The Monotreme Eye, 664 — The Monotreme Retina, 669 —

The Marsupial Eye, 671 — The Marsupial Retina, 674.

B. Placentals 675

The Eye as a Whole, 676— The Retina, 684— The Early
History of the Placentalian Eye, 686.

BIBLIOGRAPHY 693

INDEX AND GLOSSARY 721

xiv

Part I -Basic

Chapter 1
LIGHT AND ITS PERCEPTION

The principal means by which most animals are made aware of their
surroundings, and changes in these surroundings, is the reflection or
emission of light toward them by external objects and the reception of
this light by special organs which we term photoreceptors. The more
complicated of these photoreceptors are called eyes, though it is not
complexity, as such, which governs the applicability of that special term.
We say that the function of the eye is vision, but since all photoreception
is not vision and not all photoreceptors are eyes, we must consider these
broader and narrower terms before delving into our subject proper —
the structure and variations of vertebrate eyes and their relation to the
ways of life of their possessors.

Light may best be defined, for our purposes here, as a rhythmic eman-
ation of energy whose rhythm-frequency or pitch falls within definite
limits, outside of which are the higher or lower frequencies of radio,
cosmic, X-, and other rays. Visible light thus forms a circumscribed
band of frequencies to which the eye happens to be sensitive and which,
compared with all forms of radiant energy in general, is like a single
octave toward the high-pitched end of the scale of a piano (see Table I) .
It contains only a small fraction of the total amount of energy given off
by the sun, and sunlight in turn forms only a portion of the 'grand
spectrum' of radiant energy. Like other forms of radiant energy, light
in its ultimate units can vary in but simple ways — in speed, in frequency,
and in intensity. But natural lights and illuminations are complex mix-
tures of these variations, and make possible the infinite variety of nature's
pictures, varying in tone or shading (owing to combinations of inten-
sities) and in color or hue (owing to combinations of frequencies) ,

We have been discussing light as an objective physical entity; but, just
as there would be no sound if a tree were to fall with no one to hear it,
so also there would be no light in the physiological sense if there were no
photoreceptor upon which it impinged. In this other sense light is a
sensation, an experience in consciousness. Like other such experiences,
it may be evoked by a limited number of causes (other than actual

2 LIGHT AND ITS PERCEPTION

physical light) . The qualities of a light-sensation bear only a close, not
an absolute, relationship to the objective attributes of a physical light
which produces it. Thus, different colors may be seen under special cir-
cumstances when the corresponding different frequencies of light are
not being steadily presented to the eye at all, or the same color may
result from totally different mixtures of frequencies. Two lights with the
same energy-content may appear different in brightness while two others,
equally bright, may differ greatly in actual physical intensity. Color and
brightness are thus subjective correlates of the objective frequency and
intensity. The former can be perceived but not measured, while the latter
can be measured with inanimate instruments but cannot be perceived
with the eye.

A sobering array of optical illusions may be seen by the reader in any
good reference work on psychology, and will serve to teach, still more
emphatically, the lesson that: "Our eyes do not see; but we see with our
eyes." Photoreception is one thing — it may be conscious, the reception
of the external stimulus of light upon the sill of the "window of the
soul" — or it may lead reflexly to quite unconscious activities such as the
change of the size of the pupil, the aiming of the eyes, the blinking of
the lids when the eye is about to be struck by something, and so on.

Vision is something more. It is the complex and sometimes deceptive
product of the interaction of the simple information which travels along
the optic nerve and the manipulations, as yet unfathomable, which this
information undergoes in the brain before it is presented to the con-
sciousness for action or other disposal.

A photoreceptor may be constituted by a single part of a one-celled
animal; by one of a number of similar, scattered, photosensory cells in
an invertebrate's skin; by a patch of cells closely aggregated into a plate,
or lining a pit; or by an ocellus or eye (Fig. 1). This last term is best
reserved for those photoreceptors in which there is a light-sensitive layer
of cells upon which accessory parts converge the light rays received from
environmental objects. An eye, then, ordinarily contains at least a photo-
sensory epithelium or retina, and a lens. An image may however be
formed upon the retina by a pinhole (as in the chambered nautilus)
instead of by a lens; or, the lens in a given type of eye may be employed
to concentrate the light in order that the eye may work in dimmer illum-
inations, instead of to form an image so that the mind may have a picture.
Finally, a number of 'concentrator' units may be congregated so that a
mosaic image can be built up in the consciousness itself, and it is upon

OBJECTIVE AND SUBJECTIVE LIGHT 3

this plan that the 'compound' eyes of many arthropods are constructed.
Vertebrate eyes are all built upon one fundamental plan. With the
exception of those which have degenerated because their owners live
underground, or in the perpetual night of caves or the depths of the
ocean, they are provided with a retina and with a lens whose optical
properties are such that it forms an image upon the retina. The lenses of
the median eyes which some reptiles possess on the top of the head are
probably often of the concentrator type; but those of the lateral, or
ordinary, eyes are nearly always eikonogenic — that is, image-forming.

c n^

Fig. 1 — Various photoreceptors.

a, intracellular type in a one-celled animal, Pouchetia cornuta. b, scattered photosensory
cells in the skin of an earthworm, c, pit-like visual organ of a limpet, Patella, d, pinhole-
camera type of eye in the chambered nautilus, e, ocellus of a scorpion, Euscorpius, with
concentrating lens, f, eye of a snail, Murex. g, image-forming eye of a squid, Loligo.
h, eye of vertebrate.

c- cuticle; e- epithelium; /- lens; n- nerve fibers; p- pupil; r- retina; s- secreted material.

Before we pass to a consideration of the detailed structure and work-
ings of a standard vertebrate eye, it needs to be further emphasized that
vision, seeing, is a phenomenon of the mind plus the eye and not of the
eye alone. It would probably not stagger any reader of this book to be
asked to believe that a worm may react to a light-stimulus without having
a sensation or consciousness of light. Vertebrate vision as we ourselves
experience it, however, is more than just photoreception. Vertebrate
visual mechanisms, from fish to mammal, are so nicely constructed that
so far as the eyes themselves are concerned, they may in many cases send

LIGHT AND ITS PERCEPTION

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VISION VERSUS PHOT ORECEPT ION 5

to the central nervous system all of the information that human brains
receive from human eyes. That does not mean at all, however, that the
same use and value is ever made and obtained from that information.

Many vertebrates with perfectly good eyes, as complex as our own,
may not see anything. In explanation of this perhaps surprising state-
ment, it may be enough to point out that the portion of the brain in
which human visual impulses terminate and are integrated — in which,
in other words, vision seems to reside — is not present in the brains of
fishes at all. A fish may have a knowing look in his eye as he passes up
one kind of fly and avidly seizes another, but we have no right whatever
to assume that he sees either fly, or indeed anything else. It is quite
possible that he is acting, like the worm, only reflexly and without con-
scious accompaniments to patterns of shade and hue which, given a
brain capable of the analysis ours can perform, would be mental pictures
to him as they are to us.

When therefore, elsewhere in this book, such questions are raised as :
"Do dogs see colors?" and "Can fishes tell a square from a triangle?"
the reader must visualize 'see' and 'tell' in tell-tale quotation marks, and
bear with the writer if he seems to lapse into anthropocentrism and to
attribute conscious visual acts to animals whose dim minds we cannot
read. It is easiest to compare the visual potentialities of one ocular
mechanism with those of another as though behind each there lay a brain
like that of man; but it is hoped that without further frequent reminder,
the reader will forever remember this :

Human vision, so valuable and so kaleidoscopic, is the product of a
complex brain teamed with a relatively simple eye; and when we some-
times encounter more complex eyes (which are always connected with
simpler brains) we must not assume that they afford their owners any-
thing so informative of the environment as does the vision we experience.
"Nothing is in the mind which is not first in the senses" — but the sense-
organs, and particularly the eye, may offer the mind much more than
the latter can assimilate.

Chapter 2

A TYPICAL VERTEBRATE EYE: THE HUMAN

(A) Structures and their Functions

The human eye will serve admirably as an introduction to vertebrate
ocular morphology and physiology, for it is fairly well generalized and
presents no bizarre features. In the ensuing discussion, fine structural
and terminological details will be given only where they are important
for an understanding of the workings of the eye. Any detailed descrip-

y/////////////////////////A

V///////////////////////77,

Fig. 2 — Comparison of eye and camera.

Parts which correspond in function bear similar numbers. /- retina = film, on curved track;
2a- cornea = front element of lens; 2h- crystalline lens = rear element of lens; j- iris :z dia-
phragm between lens elements; 4- pigment of chorioid coat = flat black paint; 5- eyelids =
roller-blind shutter.

tion of the human retina will be omitted here, since a general treatment
of the vertebrate retina is given in Chapter 3. The reader who wishes to
learn the histology of the human eye for its own sake will of course study
actual preparations and a textbook of microscopic anatomy.

The Eye a 'Camera' — It is almost a cUche to say that the eye is built
like a camera (Fig. 2) . In each there is a sensitive screen (retina = film
or plate) on which an inverted image is formed by a lens (corneas-
crystalline lens = lens). One device (lids = shutter) can exclude light,
which when admitted by it is regulated in amount by a variable aperture
(pupil = diaphragm aperture). The interior is darkened (chorioid pig-
ment = dead black paint) so that internal reflections will not blur or

THE EYE A 'CAMERA'

multiply the image. Lastly, the whole apparatus can be set to take
equally sharp pictures at different distances (accommodation = substi-
tuting one lens for another in the camera, or varying distance between
lens and film).

posterior chamber
limbal zone.

conjunctiva
canal of Sc hie mm
ciliary muscle

sclera
chorioid'

lamina cribrosa

Fig. 3 — Horizontal section of right human eye. x 4. Modified from Salzmann.

On the left, the section contains a cihary process behind which the zonule fibers are partly
concealed; on the right, the section has passed between two ciliary processes and the full
extent of the zonule fibers can be seen. The limbal zone (transition between cornea and
sclera) is stippled to emphasize that it is broader internally than externally.

The Fibrous Tunic — The outer case of the living camera is formed
by the fibrous tunic, consisting of the sclera and the cornea, the latter
seemingly a transparent anterior continuation of the sclerotic coat which

8 A TYPICAL VERTEBRATE EYE: THE HUMAN

is more sharply curved than the latter (Fig. 3). A substantial portion of
the thickness of the cornea represents the skin of the head, which during
evolution became affixed to the eyeball, leaving loose places, to permit
eye movements, up underneath the eyelids where it merges with their
linings to join the ordinary outer skin at the lid margins. Only some of
the inner layers of tissue in the cornea represent a clear window in the
original, ancestral, fibrous capsule. As a matter of fact, the sclera itself

Fig. -I — Fibrous and vascular tunics of the human eyeball, x 135.
Modified from Maximow and Bloom, after Schaffer.

a, sclera and chorioid.

a- artery; c- choriocapillaris layer of chorioid; Iv- lamina vitrea; s- sclera; v- vein; vl- vascular,
pigmented layers of chorioid.

b, cornea.

b- Bowman's membrane; d- Descemet's membrane; e- epithelium; m- mesothelium; p- sub-
stantia propria.

is almost as transparent as the cornea in many of the lower vertebrates.
The 'white' of the human eye is differentiated from the clear cornea not
because the latter has become transparent secondarily, but rather because
the sclera has become clouded. What has happened in evolution also
takes place in individual development, and the clear parts of the em-
bryonic eye are clear from the start and remain so — they do not become

THE FIBROUS TUNIC 9

SO. Despite this easily ascertained fact, many speculations have been
made as to what factor is responsible for the transparency of the cornea
and the lens. The really interesting question is, what makes the other
tissues of the developing embryo become opaque.

The sclera (Fig. 4a, s) is composed of tough, inelastic, tendinous tissue
organized in ribbon-like bundles of microscopic fibers which are felted
together in such a way that the whole tissue is about equally strong in all
directions — to resist the intraocular pressure, equal of course in all direc-
tions, without allowing the eyeball to change its shape. The flat fiber-
bundles are of unknown length, for their ends cannot be found; but each
seems to arise somewhere behind the rim of the cornea, runs parallel
thereto for a space, then courses backward around the eye and forward
again in a wide loop — not, however, following a great circle of the ocular
sphere. The tissue of the sclera contains very few cells. It consists chiefly
of the lifeless fibers, and its rate of living (metabolism) is so low that
it requires no direct blood supply. Nearly all of the blood vessels to be
seen in sections of the sclera are merely passing through it on their way
into or out of the chorioid coat.

The layers of fibers in the cornea (Fig. 4b) are not so much felted
as in the sclera, but run more nearly parallel with less interchange of
fibers between layers. The cells between them are consequently more
definitely organized into layers also; but they are scattered very far apart
in a given layer. The substance of the healthy cornea is quite devoid of
blood vessels, which would interfere with transparency. At the same
time, it is so firm that the diffusion of liquids through it is much im-
peded. Its living cells, the corneal corpuscles, therefore join hands by
means of long, delicate threads of living protoplasm along which nutri-
ments and wastes may be transported to and from the blood vessels
surrounding the margin of the cornea. The avascularity of the cornea,
and evaporation from its surface, make it several degrees cooler than the
body as a whole, and the metabolism of the corneal cells is adjusted to
the lower temperature.

The change in the character of the tissue, as one passes from the sclera
into the cornea, is a gradual one and the wide region of transition noted
marks the limbus (rim) of the cornea. A flange of scleral substance, the
scleral roll, (Fig. 5, sr) overlaps the edge of the cornea on its inner sur-
face so that the illusion of the cornea being set in the sclera, like a watch-
crystal in its bezel, is created. The two portions of the fibrous tunic are
not actually at all easily separable, but the limbus is the weakest region

A TYPICAL VERTEBRATE EYE: THE HUMAN

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THE FIBROUS TUNIC 11

in the fibrous tunic. It is at the Umbus that an isolated eyeball will
rupture, if it is squeezed until it bursts.

The outer surface of the fibrous mass (substantia propria) of the
cornea is covered by a stratified epithelium which is much like that lining
the mouth, and lacks the dead, homy outer layers which are present on
the general epidermis of the body. This corneal epithelium (Fig. 4b, e;
Fig. 5, ce) is continuous, at the limbus, with the thicker and less regular
epithelium of the conjunctiva (Fig. 5, ec). The conjunctiva (Fig. 5, co)
represents head skin which at the margins of the upper and lower eyelids
is doubled back on itself up underneath them to form their linings, and
is continuous over the front of the eyeball, with which it is fused to form
the 'conjunctiva fixa' — the loose folds in the culs-de-sac up under the
lids being the 'conjunctiva libera'. The connective-tissue dermis of the
conjunctiva fixa can hardly be distinguished from the loose connective
tissue which clings to the sclera; but at any rate it stops at the limbus
and only the epidermis appears to continue over the cornea.

Actually the dermis belonging to the corneal-epithelium part of the
conjunctiva is represented by some of the outermost layers of the sub-
stantia propria — no one can say just how many, in the case of the human
eye. The very outermost layer, just beneath the epithelium, is devoid of
cells and stains a little differently. It is known as Bowman's membrane
(Fig. 4b, b) ; but it scarcely deserves recognition and in the lower animals
cannot ordinarily be made out at all as a distinct part of the substantia
propria.

The corneal epithelium is richly supplied with pain-sensory nerve end-
ings and apparently with no others, and is remarkable for the speed with
which it can grow to repair or replace itself if injured. There is some
reason to think that it is normally nourished from entirely outside the
body — from the tears, which contain appreciable amounts of nutrient
substances.

The inner surface of the cornea is lined by a thin pavement of cells
usually called the endothelium of the cornea. (It more properly deserves
to be considered a portion of the mesothelium of the anterior chamber,
however, since it is continuous with the anterior covering of the iris and
the term 'endothelium' is outmoded as applying to mesodermal epithelia
generally). Between the substantia propria and the mesothelium, and
secreted by the latter as its basement membrane, is the thin, homo-
geneous, elastic 'membrane of Descemet' (Fig. 4b, d).

12 A TYPICAL VERTEBRATE EYE: THE HUMAN

It needs to be made clear at this point that the adjective 'elastic',
wherever it is appUed to an ocular structure, means 'springy' rather than
'easily stretched' — thus Descemet's membrane, the lens capsule, the
zonule fibers and so forth are elastic in the sense of a celluloid strip,
not of a rubber cord.

The Intra-Ocular Fluids — The fibrous tunic is normally kept dis-
tended to the point of rigidity by the pressure of fluid secreted within
the eye. This fluid, the aqueous humor, is continuously produced at a
slow rate and drained out of the eyeball into the blood stream by a
complex arrangement which is so regulated that the intra-ocular pressure
remains roughly constant at about 25 millimeters of mercury. Half of
this internal pressure is created by the external pressure of the extra-
ocular muscles and if both these and the blood-vessels leading to the eye
are severed, the mtra-ocular pressure falls to about 10 millimeters of
mercury. Overproduction of aqueous humor or any chemical, mechan-
ical, or pathological upset in the drainage system will lead to a painful
rise in pressure, the condition being known as glaucoma. If the pressure
is unrelieved, it clouds the cornea and injures the retina, and the end
result is blindness.

The greater portion of the intra-ocular fluid, occupying the large
chamber in the back of the eye, is rendered gelatinous by the addition
to it of proteins secreted during development by the retina. This mass
of gelated aqueous is called the vitreous (= glassy) body, or vitreous
humor (Fig, 3; Fig. 5, r). It is relatively permanent and in the fully
grown eye it is fixed in amount, so that any portion of it which is lost
through a wound is replaced only by watery aqueous humor. It is mostly
to the unmodified aqueous, in the front of the eye, that fresh fluid is
constantly added; and it is with the liquid aqueous that the pressure-
regulatory drainage mechanism — the canal of Schlemm (Fig. 3; Fig 5,
sc) communicates in an indirect way.

So far as the human eye itself is concerned, there is no powerful
reason why the material which fills the chambers of the eye should be
of two kinds — liquid anteriorly and semi-solid posteriorly. But in the
forebears of the fishes, which invented the vertebrate eye, the material
near the cornea had to be kept fluid so that the lens could be readily
moved in accommodating the focus of the eye to different distances,
and the lens would have dropped back into the globe if there were
only liquid behind it. In the higher vertebrates, the lens is not changed

HUMORS; UVEAL TRACT 13

in position but only slightly altered in shape, and it is held firmly in
place by ligaments which the lower fishes lacked; but the differentiation
in consistency of the intra-ocular media has never been abandoned. This
is probably fortunate, as otherwise, in animals above the fishes, the evolu-
tion of a muscular iris and mobile pupil might have been inhibited.

The Uveal Tract — The layer of the eyeball wall next inside the fibrous
tunic, clinging closely to the sclera but swinging inward away from it at
the sclero-corneal junction, is the uveal tract or uvea. The part of the
uvea which is attached to the sclera is a thin, deeply pigmented layer
consisting mostly of blood vessels, with connective tissue binding them
into a membrane. It is called the chorioid coat (Fig. 3; Fig. 4a). The
pigmentation of the chorioid prevents internal reflections and keeps light
from getting through the wall of the eyeball indiscriminately, and the
rich vascularity of the tissue is concerned with the nutrition of the highly
metabolic retina.

Against the inner surface of the uveal tract, throughout its extent,
lies the retina (Fig. 3). Where it is in contact with the chorioid, the
retina is thick (pars optica) and is sensitive to light. The anterior por-
tions of the uveal tract are lined with a thin, insensitive continuation of
the retina (pars caeca), which thus really terminates at the rim of the
pupillary aperture.

The sensory part of the retina has the form of a cup whose lip, the
'ora terminalis' (Fig. 3; Fig. 5, oO, is an important landmark inside the
eyeball. From the ora forward, both retina and uvea are profoundly
modified. The chorioid, at that point, thickens and ceases to be so
heavily pigmented and vascularized. The thickened region forms, in a
sagittal section, a slender triangle with its narrow angle aimed pos-
teriorly to merge into the chorioid. This thickened zone of the uvea is
called the ciliary body (Figs. 3 and 5), and it is characterized by the
presence of many involuntary muscle fibers and, on its inner surface
anteriorly, a large number (70-80) of radially arranged fin-like struc-
tures, the ciliary processes. Each ciliary process (Fig. 3; Fig. 6c; Fig. 7g)
is essentially a fold of non-sensory retina covering both sides of a flat
sheet of small blood vessels. Retina and uvea thus intimately cooperate
to form the ciliary processes. The anterior part of the ciliary body which
bears them is termed the corona ciliaris. At the posterior ends of the
processes they diminish in height and fade down to the level of the val-
leys between them. This leaves, between the hind ends of the processes

14 A TYPICAL VERTEBRATE EYE: THE HUMAN

and the ora terminalis, a fairly smooth posterior region in the ciliary
body, called the orbiculus ciliaris (Fig. 3 ; Fig. 5, oc; Figs. 6c, 7g, cor, orb) .
Inasmuch as it is from the blind epithelial part of the retina covering
the ciliary body that the aqueous humor is given off, the ciliary processes
and the less conspicuous secondary folds between them are best inter-
preted as a device for greatly increasing the secretory surface for the

MiS

spca
spcv

Fig. 6 — Vascular structures of the human eye.

a, vascular plan of the eye, showing veins in black, arteries clear. Modified from Adler,
after Leber.

dcv- anterior ciliary vessels; cc- choriocapillaris; crv- central retinal vessels; c/- canal of
Schlemm; ey- episcleral vessels; Ipca- long posterior ciliary artery; mc- major circle of iris;
pcy- posterior conjunaival vessels; rca- recurrent chorioidal artery; rv- retinal vessels; spca-
short posterior ciliary artery; spcv- short posterior ciliary vein; yep- vessels of ciliary process;
y'l- vessels of iris; yns- vessels of optic nerve and sheath; yy, yy- vorticose veins.

b, surface view of portion of choriocapillaris from fundus, x 65. Redrawn from Salzmann.
The black spots mark the junaions, with the capillary net, of small connecting arteries and veins.

c, surface view, from inner side, of portion of ciliary body. After Franz.

c- cornea; ch- ciliary body; cor- corona ciliaris; cp- ciliary processes; /, /- minor folds; ;'- iris;
orh- orbiculus ciliaris; r- retina; s- sclera.

production of aqueous. This was probably not their primary function
when they were originally evolved, however, as will be seen later when
the method of accommodation in the reptiles is explained. Over the cili-
ary body, the blind pars ciliaris retinae consists of a double layer of tall
cells, the ciliary epithelium (Fig. 7g, ce, ce). The outermost of these
layers is pigmented and is a simple continuation of a similar pigmented
layer which, further posteriorly, lies between the chorioid and the sensory

THE UVEAL TRACT

a V abl pbl

Fig. 7 — The iris.

a, radial section of human iris, x 24. a- artery; at/- anterior border layer; c- crypt; «e- iris
epithelium (= pigmented posterior layer of iridic retina); ma- major circle (circular artery in
ciliary body); wj- minor circle (anastamosis of radial vessels); phi- posterior border layer
(= dilatator pupillee, = myoid lamina of anterior epithelial layer of iridic retina); pz.- pupil-
lary zone (remainder of iris constitutes ciliary zone); s- connective-tissue stroma; sm-
sphincter muscle; v- vein.

b, =the small rectangle in a, enlarged to show the heavily pigmented posterior epithelium
and the lightly pigmented 'spindle cells' of the anterior epithelial layer, whose muscular
portions merge into a sheet to form the dilatator. Partly after Salzmann.

c, a spindle cell from the anterior retinal layer of the iris of a rhesus monkey, showing the
epithelioid cell-body and the partial differentiation of the base of the cell into a muscle
fiber, which is shown in its contracted condition. Redrawn, modified, after Hotta. d, same
as c, relaxed, e, same as c, but stretched (as when sphincter contracts).

f, diagram of vascular plan of mammalian iris, showing veins in black, arteries clear.
cp- capillary plexus of pupillary zone (devoted particularly to the sphinaer muscle); Ipca,
Ipcd- long posterior ciliary arteries; ma- major circle; wi- minor circle.

g, diagram showing distribution of pigment (stippling) in the retinal portion of the iris, as
compared with that in the ciliary epithelium and in the region of the sensory retina.
ce, ce- ciliary epithelium; cor- corona ciliaris; cp- ciliary process; ie- iris epithelium; o- era
termmalis of sensory retma; orb- orbiculus ciliaris; pbl,sc- piosterior border layer ( = dila-
tator) and spindle cells; pe- pigment epithelium of sensory retina; s- sclera; sm- sphincter
muscle; sr- sensory retina; u, u- uvea.

16 A TYPICAL VERTEBRATE EYE: THE HUMAN

part of the retina throughout their extents. The innermost of the two
layers of the ciliary epithelium is unpigmented and is a forward con-
tinuation of the sensory retina, which drops sharply in thickness at the
ora terminalis (Fig. 3; Fig. 7g).

At the anterior end of the ciliary body the uveal tract bends sharply
inward, away from the fibrous tunic, to form the iris (Figs. 3, 5, and 7).
This structure is an opaque disc of tissue with a hole, the pupil, in its
center. It is not flat, but bulged slightly forward by the lens which lies
behind it, so that the iris forms a low truncated cone when seen in profile.
The periphery of the iris is anchored to the inner aspect of the limbus
corneas by a connective-tissue meshwork, this region being known as the
iris- or filtration-angle (Fig. 5, mt, fa). It is important that this crevice
between iris and cornea remain wide, and not be squeezed shut or
blocked by material of any kind. This would lead to glaucoma, for the
only important exit-pathway for excess fluid, the canal of Schlemm (Fig.
3; Fig. 5, sc), lies shallowly embedded in the fibrous tunic at the iris
angle, separated from the aqueous only by a thin layer of the meshwork
tissue.

In the iris, the uvea and retina are even more intimately associated
than in any part of the ciliary body. On the posterior surface of the iris
— that is, the surface directed toward the lens and the vitreous — the
relations of the pigmented and unpigmented layers of the double retinal
epithelium (here called the pars iridica retinae) are reversed; for here
it is the innermost or posterior layer, nearer the lens, which is pigmented.
The anterior or outer layer, toward the cornea, contains little or no pig-
ment (Fig. 7g). In blue eyes, the brown pigment of the retinal backing
of the iris is the only pigment the iris contains — the blue color of the iris
being caused by optical trickery similar to that which makes veins, con-
taining dark red blood, appear blue when seen through white skin. In
brown and black irides, there is more or less pigment also in the uveal
connective-tissue stroma of the iris (Fig. 5, is; Fig. 7a, s), which is much
like the chorioid in construction. Inasmuch as the usual color of the
mammalian iris is brown, and the human blue eye represents a failure to
develop stromal pigment, the blue eye may properly be considered an
abnormality — a developmental anomaly — despite its common occurrence.
This viewpoint is strengthened by the fact that blue eyes are recessive to
the darker colors in heredity. The reader is not advised, however, to
refer slightingly to the azure orbs of his inamorata! Perfect albinos
(which perhaps never occur in the human species) of course lack even

THE PUPIL 17

the retinal pigment, hence have pink irides owing to the easy visibihty
of the numerous blood vessels of the iris.

The Pupil — The function of the iris is to 'stop down' the lens (Fig. 2)
— to prevent the light coming in through the peripheral zone of the
cornea from passing through the edge of the lens and reaching the retina.
Only the central part of the lens is optically good, and within certain
limits the image on the retina will be sharper, the smaller the aperture
in the iris. At the same time, the image will be less bright with a smaller
pupil, and in a given illumination might not be intense enough to affect
the retina unless the pupil could be opened more widely. A wide dila-
tation of the pupil affects the illumination of the image more than its
area or the size of the visual field it subtends; but this increase in image
brightness entails a sacrifice of the clarity of the picture, owing to the
optical imperfection of the lens periphery which is brought into play.
The regulation of the size of the pupil, in sympathy with the vari-
ations in the sensitivity of the retina and the external illumination, is
accomplished by contractile elements in the iris. Some of these are full-
fledged involuntary muscle cells, indistinguishable from those of the
abdominal organs, and are organized into a ring-shaped 'sphincter
pupillje' embedded in the iris stroma and closely surrounding the pupil
{sm in Figs. 5, 7a, 7g). Contraction of this muscle reduces the diameter
of the pupillary circle, though of course there is an obvious minimum
below which it cannot be further reduced; so, a circular pupil like that of
man cannot be closed entirely. The antagonist of the sphincter is a com-
plex consisting of the elasticity of the tissue and the radial blood vessels
(Fig. 7f) of the iris (which are straightened out when the sphincter con-
tracts and which tend to return to an undulant resting shape) together
with the active contractility of the 'dilatator pupillae'. This latter (Fig.
7a, pbl; Fig. 7b-e) is not a true muscle, but a myoid lamina developed
from the anterior face of the pars iridica retinae : the sparsely pigmented
cells of the anterior layer of this epithelium have each a long spindle-
shaped portion containing contractile fibrillae and lying with its long axis
at right angles to that of the cell body, which is attached to the middle of
the spindle (Fig. 7b-e) . These spindles thus form a layer which appar-
ently lies alongside the anterior layer of epithelium (Fig. 7a, pbl) in the
pars iridica retinae, but is really a part of that epithelium (Fig. 7g) . The
spindles may even be fused with each other in a syncitial fashion, though
this point is uncertain. Their myofibrillae run radially in the iris, so that

18 A TYPICAL VERTEBRATE EYE: THE HUMAN

their contraction opens up the pupillary aperture, throwing the body of
the iris into concentric folds or contraction furrows. The dilatator, being
only a part of an epithelial layer, contains no nuclei and no blood vessels,
nor any connective tissue forming septa within it or a sheath outside it.
The sphincter shows all of these features, however.

Both sphincter and dilatator are derived embryologically from the
anterior layer of the double epithelial pars iridica retinae which is, em-
bryologically, the zone of the optic cup nearest its lip. The cells which
become sphincter muscle fibers separate completely from the epithelium
late in fetal life, and the epithelium exhibits a gap underneath them (Fig.
7a, g) ; but the dilatator cells remain permanently, so to say, in a half-
way stage of conversion from epithelium into muscle. As a rare anomaly
in man, even this development may fail and there may be no trace of a
dilatator, the pupil then remaining strongly contracted throughout life
('microcoria'). Wherever among the lower animals the dilatator is lack-
ing (the pupil then being opened by the elasticity of the iris tissue alone,
upon relaxation of the sphincter) the spindle cells of the anterior layer
of the pars iridica retinae remain wholly epithelial, like the cells of the
posterior layer, and fail to lose their pigmentation during development as
do the elements which produce dilatator fibers in other animals and man.

The sphincter and dilatator have very different nerve supplies from
the autonomic system, and respond very differently to pharmacological
agents and to substances which duplicate or imitate the natural chemical
intermediators between nerve and muscle. They are involved in a num-
ber of reflexes. The fundamental one is the contraction of the pupil to
protect the retina from dazzlement when the external illumination is
suddenly increased. As the retina adapts to the new illumination (by
reducing its sensitivity) the pupil slowly reopens. Other reflexes include
the 'consensual' contraction of the pupil of a covered eye when the other
eye is illuminated, its dilatation in emotional states or when the skin of
the neck is pinched, its contraction when the eyes converge and accommo-
date for nearby objects, etc. The last-mentioned of these reactions is not
a true reflex, but the result of co-innervation of the sphincter pupillae
and the muscles of accommodation, the common nerve also running
with that which supplies the convergence-muscle, the internal rectus. The
complexity of some of the pupil reflexes is only realized when an attempt
is made to analyze their neurological basis in cases where the reflexes
have been lost or altered, due to traumatic or pathological lesions in the
central nervous system.

THE LENS AND ZONULE 19

The Lens and Zonule — The crystalline lens is a glassy, cushion-
shaped body which lies behind the iris (Figs. 3 and 5). It is supported
from behind by the vitreous body and from the front, to some extent,
by the iris. The slightly conical form of the iris is entirely owed to the
light pressure of the lens against it. If the lens is removed, as in an oper-
ation for cataract, the iris thereafter hangs loosely and trembles when-
ever the eye moves.

The chief support of the lens is given by a great number of firm
threads which, like so many guy-ropes, run from the rim of the lens to
the ciliary body. Collectively, these threads form the suspensory liga-
ment or zonule of Zinn (Fig. 3; Fig. 5, ^/). Each zonule fiber arises from
the surface of the ciliary epithelium, runs forward between two adjacent
ciliary processes, and sweeps around toward the lens equator to fuse with
the capsule of the lens. The largest number of fibers insert on the an-
terior face of the lens near the equator, a rather smaller number on the
posterior face, also near the equator; and scattered fibers insert at the
equator everywhere between these anterior and posterior sheets of fibers
('anterior and posterior leaves of the zonule'). Some atypical fibers cross
each other between the zonule leaves, and others run from one ciliary
process to the next and do not join to the lens at all. A little behind
the posterior zonule leaf (which is bowed to fit its curvature) lies the
anterior membranous surface of the vitreous, which is joined to the pos-
terior lens capsule along a narrow ring (Egger's line; Fig. 5, el) but is
free of the posterior lens surface in its center, creating the fluid-filled
'retrolental space' (Fig. 3; Fig. 5, rs). Between the anterior hyaloid mem-
brane of the vitreous and the posterior leaf of the zonule is the flattened
annular 'canal of Petit'. Between the leaves of the zonule is the space
called the 'canal of Hannover' — though of course it is not a true canal
since the fibers in each leaf of the zonule do not form an intact mem-
brane, but rather a grille. Between the anterior leaf and the back of the
iris lies the posterior chamber sensu stricto (Fig. 5, pes), although the
term 'posterior chamber' is properly enough used to embrace collectively
all of the aqueous-filled spaces behind the iris.

Newly-formed aqueous, poured into the posterior chamber by the
ciliary epithelium, can get into the anterior chamber (between iris and
cornea) only by infiltrating between the zonule fibers and then passing
between lens and iris and through the pupil. If, in an inflammation of
the iris, the whole pupil margin adheres to the lens capsule, the aqueous

20 A TYPICAL VERTEBRATE EYE: THE HUMAN

accumulates in the posterior chamber and bulges the iris forward, this
being one of the many possible causes of glaucoma.

The body of the lens, released from its capsule in the fresh condition,
is a glutinous, almost inelastic mass which gives no hint of its true
histological structure. This is best disclosed by crushing a lens which has
been hardened in formalin or alcohol, when it is seen that the lens is
composed of innumerable layers, like the coats of an onion, each layer
in turn being made up of fine fibers. An individual lens fiber in a given
layer runs from an anterior point, near the axis of the lens, circumfer-
entially around to a point in the posterior half of the lens — again near
the axis. No fibers could each have both ends exactly on the lens axis,
or the lens would be greatly elongated, pointed anteriorly and poster-
iorly, and would then be quite unsuited to its optical function. Fibers
running in one radius or meridian of the lens meet fibers in the diamet-
rically opposite meridian, end-to-end, along radial planes called 'lens
sutures' (see Chapter 5, section A; Figs. 40, 41, pp. 110-1). These suture
planes necessarily branch more and more elaborately as the lens body
grows by the addition of new layers of fibers at its surface, in order to
accommodate the increase in number of fibers in each layer over the
smaller number in the next innermost, slightly older layer, A given lens
fiber tends to lie along the convex curvature of a fiber in the next inner-
most layer of fibers, and along the concave curvature of one in the next
outermost layer. Radial lamellae of fibers are thus built up so that the
lens, besides having an 'onion' aspect, can also be thought of as being
built like an orange with many hundreds of segments. Since the diameter
of a single fiber is quite constant, the number of fibers per layer in-
creases as the lens grows, and the number of radial lamellae perforce
increases from time to time so that a maximum can be counted at the sur-
face, fewer and fewer farther and farther in toward the center of the lens.

The lens is contained in an unbroken, homogeneous, elastic envelope,
the lens capsule. The capsule is not uniform in thickness everywhere but
has definite thickened zones at particular locations, whose importance
will be explained in connection with accommodation. Covering the an-
terior half of the lens, to and slightly beyond the equator, is a single
layer of cuboidal cells, the lens epithelium (Fig. 5, le). This layer lies
just beneath the capsule. It is of no importance optically, but is all-im-
portant for the growth of the lens. It is believed to secrete the capsule
or at least to be more efficient in this than the lens fibers which have
their sides against the posterior half of the capsule, for the anterior por-

THE LENS AND ZONULE 21

tion of the capsule is thicker than the posterior in most animals. This
is, however, open to interpretation as a positive adaptation rather than
a mere accident of difference in secretory capacity, for as will be seen
later, accommodation is facilitated by a thick anterior capsule but would
be indifferent toward an equally thick posterior capsule.

The lens epithelium is the source of all of the myriads of lens fibers
excepting a very small ball of them at the center of the lens, which are
formed directly from the posterior wall of the embryonic lens vesicle —
a bubble of tissue which forms as a pit in the skin of the head, from
which it closes off and pinches free to sink down into the optic cup. If
the lens epithelium could be isolated intact, it would be like a thin,
shallow bowl composed of tiny tiles. We must imagine this bowl to be
growing constantly by the multiplication of its tiles, with those at the
edge of the bowl elongating into rods which, as they get longer and
longer, each slide one end along the inner surface of the bowl toward
its center, the other end growing in the opposite direction and curving
toward a point in space above the center of the bowl. It is in this fashion
that each new layer of lens fibers is added over the preceding one (Figs.
40 and 41), by the conversion of the epithelial cells at the equator of
the lens into long, curved threads which are hexagonal in cross-section
so as to fit against one another without intervening space, just as do the
cells of the epithelium itself. Any given cell in the epithelium of a grow-
ing lens is thus moved steadily toward the lens equator by the mitotic
expansion of the epithelium, and, upon finding itself eventually at the
rim of the epithelial bowl, proceeds to convert itself into a lens fiber.

The lens is very prone to opacify, thus giving rise to 'cataract', in re-
sponse to any of a number of causes; but it is normally optically empty —
that is, completely transparent and with no obvious signs of its elab-
orate internal structure. With special lighting arrangements, as with the
ophthalmologist's slit-lamp, it is possible to see several concentric sur-
faces within the lens, analogous to growth-rings in a tree trunk. These
mark periods in life — the same in all of us — at which the optical density
of the new-forming lens fibers is changed abruptly to a lower value than
that of the previously formed layers of fibers. Thus the optical density of
the lens — its effectiveness in slowing the speed of light and hence its
focusing power — decreases in several distinct steps from center to sur-
face. In a given region, however, the density of the fibers and of '"he
scant fluid between them is so nearly identical that the surfaces of the

22 A TYPICAL VERTEBRATE EYE: THE HUMAN

fibers reflect no light and consequently are invisible in the living lens.
The fibrous structure of the lens simply disappears as does a glass bead
when dropped into a vial of oil of the same optical density as the glass.

(B) Optics and Accommodation

Refraction — The property of substances which is called their 'optical
density' has been alluded to above. The higher the optical density of a
material, the slower light is able to travel through it. Light travels fastest
through a vacuum and very nearly as fast through air, so that for prac-
tical purposes the speed of light in air is taken as the maximum. This
speed divided by the speed of light in a given substance gives a figure

°-°°' : i i i : ! i : :

\ .-mM

b ijiiiiin

\ ^ :::::::::

°%°o°°„°° %°i" ■■■■'■■ -Open ground
soldiers > vyheat :
open ground :::::::::

dspkremeft Q^ '. ': : ^°° ; -'o
:::::::: .\ o ° o '

\ 0 o °

a l::!:::::

c ;:;;;;;;; \\°:

Fig. 8 — An analogy for the refractive bending of light rays by a glass plate (see text).

which is called the 'index of refraction' of that substance referred to air
as a standard.

The effect of the optical density of a substance is to produce a bend-
ing of a beam of light which enters that substance at an angle, having
previously traversed a substance of different optical density. The amount
of the bend in the light-beam will depend upon the difference in optical
density of the two substances and upon the angle at which the beam
approaches their interface. The direction of bending will depend upon
whether the second substance traversed has a higher or lower density,
or index of refraction, than the first.

This bending of light rays when they pass through boundary surfaces
is called 'refraction'. Its basis may be best understood if we use an old

REFRACTION 23

favorite analogy for our light-beam and our pair of optically different
substances. Suppose a platoon of soldiers to be marching over bare
ground toward the edge of a wheat-field, which is at an angle to their
line of march (Fig. 8). The ranks of soldiers now represent successive
wave-fronts in a light-beam, and their files represent the individual light
rays in the beam. Obviously the soldiers cannot march as fast through
the dense wheat as over open ground, so that the latter may represent
air, and the wheat-field a piece of glass of high optical density.

As the first soldiers in the front rank start into the wheat, they are
slowed up, but those at the other end of the front rank are still able to

A

A -0- -^

f

Fig. 9 — Step-by-step explanation of the focusing of parallel rays by a convex lens.

a, displacement of ray by tilted plane-parallel plate (compare Fig. 8). b, bending of ray
by prismatic plate, c, approximation of parallel rays without convergence, by pair of tilted
plane-parallel plates, d, convergence of parallel rays by pair of prismatic plates, e, inde-
pendent foci of pairs of parallel rays, through action of prisms placed base-to-base,
■f, coincidence of foci when slope of prism faces is decreased toward their bases, g, single
focus of all parallel rays, resulting when process in f is fully carried out, yielding a
smoothly-curved lens.

march rapidly since they have not yet reached the wheat (Fig. 8a).
Consequently the front rank is swung around as if hinged at one end,
and by the time the whole of the rank is in the wheat, it has taken a
new direction of march which is of course followed by each rank in the
whole platoon (Fig, 8b). Upon emerging from the wheat-field on
the other side (Fig. 8c), the process is reversed and the platoon's line
of march becomes parallel to its original one, displaced laterally a dis-
tance which depends upon the width of the wheat-field and the difficulty
of marching through it.

24 A TYPICAL VERTEBRATE EYE: THE HUMAN

If the soldiers had encountered the wheat head on instead of at an
angle, their line of march would not have been tilted. But their ranks
would have been closed up, and while moving through the wheat each
soldier would have been treading on the heels of the man in front of him.
Strictly speaking, this would be refraction also, for the same decrease in
wavelength occurs when the angle of incidence is other than 90° —
refraction is most accurately defined in terms not of any bending of
the light rays, but of their change in speed and wavelength. Thus it
actually takes place when light meets a surface at right angles; but since
no visible change then occurs, the existence of the phenomenon is more
or less ignored.

Substituting now our beam of light and piece of glass for the soldiers
and the wheat-field, we can understand why the angle at which the light
meets the glass is so important in determining the direction the beam
will take through the glass. If the angle be changed, the new direction
will change. If a perpendicular be drawn to the surface of the glass, then
the beam of light on entering the glass from air will be bent toward the
perpendicular; and upon escaping from the glass into air again it will be
bent away from a perpendicular at the point of escape, the two bends in
the beam being equal if the two surfaces of the glass are parallel.

Action of a Convex Lens — We are now ready to understand how a
lens brings rays of light to a focus (study Fig. 9) . If a beam of parallel
rays of light strikes a convex lens, each ray in the beam will make an
angle with a tangent to the lens at the point where the ray strikes it, and
the angle will vary with the distance of the ray from the central ray of
the beam, which we will suppose to pass through the center of curvature
of the lens surface. The farther a ray is from the axial (central) ray,
the greater the angle it makes with a radius of the lens at its point of
contact with the latter, and the greater the angle of bending, toward
the radius, through which it will be refracted by the glass of the lens
(Fig. 9g).

Thus, the outermost rays of the beam are bent the most, rays lying
closer and closer to the axial ray are bent less and less, and the axial
ray is not bent at all. All the rays thus converge beyond the lens and
if the shape of the lens surface is just right, they may be made to con-
verge at a single point. This point, or 'focus', will be at a fixed distance
from the lens, and that distance can be varied only in two possible ways
— by making the lens variable in curvature or by exchanging it for a

ACTION OF A CONVEX LENS 25

different one. About the only variable lenses in the world are those in
living vertebrate eyes.

A lens forms an 'image' of an object, the distance of the image from
the lens being fixed as long as the distance of the object from the lens
is constant. We can best grasp how the image is formed if we think of
it as being made up of a large number of points, each corresponding to
a point on the object (Fig. 10). The light reflected from each point on
the object — its two end-points, say, as in Figure 10 — travels in straight
lines away from that point in all possible directions unless the object
happens to have a mirror-like surface. We can be sure of this, for we
can walk around an object and see it, from any direction, by means of

I

^ / 1 \ ^ vl/

Fig. 10 — Formation of an image by a lens.

Of the rays emanating in all dirertions from each point on the objert, those intercepted by
the lens are brought to a focus, thus generating a point in the image. Each image-point lies
on the opposite side of the lens axis from the corresponding object point; hence the image
is inverted.

the light coming in that direction from the object to our eyes. All of the
rays from an object-point which happen to be intercepted by a lens are
brought to a point focus beyond the lens at a particular, fixed distance.
If the object-point lies below the axis of the lens, however, the light from
it will be focused at an image-point above the axis and vice versa.
Hence, when we consider all the image-points formed by the focusing
of all the light from each of the object-points, we understand how the
image is built up. We also see why it hangs in space at a fixed distance
from the lens, is smaller than the object, and is inverted. We can now
see the image if we catch it on a screen at the image-distance from the

26

A TYPICAL VERTEBRATE EYE: THE HUMAN

lens. If we move the screen toward or away from the lens the image will
immediately become blurred because the object-points will be represented
on the screen not by sharp image-points, but by patches of light of the
same shape as the lens ('blur' or 'confusion' circles, where the lens is
round) which overlap each other.

If the screen now remains stationary at the proper distance, and the
object moves toward or away from the lens, the image will focus behind
or in front of the screen (Fig. 11), and the picture on the latter will
again be composed of hazy blur circles. With the object in this new
position, its image can now be made to fall on the screen only if the lens
is shifted in position or altered in curvature. Both of these methods are
used, in different kinds of vertebrate eyes, to keep the image sharp on

Fig. 11 — Relation of objea-distance to image-distance. After Kahn.

Only the B is sharply imaged on the screen, on which the A and C are represented by blurs.
The sharp images of the A and C hang in space as shown, and can be placed on the station-
ary screen only by moving the lens, or by substituting another lens of different strength.

the retinal screen when the object varies in distance from the eye. These
adjustments comprise what is called 'accommodation'.

Refractive Errors of the Eye — In the human eye there are several
curved surfaces at which refraction takes place, the end result being the
production of an image on the retina. There is also an elaborate arrange-
ment for changing the curvature of one of these surfaces so that the
image can be moved slightly forward or backward in the eye. This
mechanism of accommodation comes into play when we shift our gaze
from a distant to a nearby object, or when we watch an object which is
moving toward or away from us. As an object approaches, its image
recedes behind the retina and must be pulled forward. As an object goes
away from us, its image moves forward into the vitreous and must be
pressed back onto the retina in order to be seen sharply. In many persons
the eyeball is abnormally short (Fig. 12, top diagrams), so that the

REFRACTIVE ERRORS OF THE EYE

27

accommodation process, unaided by convex spectacles, is inadequate to
pull the image forward onto the retina and the sharp picture lies behind
the eye (hypermetropia or far-sightedness). In others, the eyeball is ab-
normally elongated (Fig, 12, bottom diagrams) and the image lies so
far forward in the vitreous (except when the object is very close to the
eye) that concave spectacles are required to move the focus of the lens
backward and place the image on the retina (myopia or near-sightedness) .

Object At Great Distance; Object At Walking Distance: Object At Reading Distance

15

o o^

tr
H o

tr —

receptive (visual-cell) layer
rays focus behind eye

some accommodation

much accommodation

rays focus in receptive layer

rays focus in receptive layer

no accommodation

some accommodation

2 —

rays focus at inner surface
of receptive layer

rays focus at outer surface
of receptive layer

rays focus in receptive layer

no accommodation

little or no accommodation

9r

rays focus in front
receptive layer

rays
of t

rays still focus in front
of receptive layer

rays focus in receptive layer

Fig. 12 — Spherical refractive errors of the eye.

Shows the extent of accommodation required, and the location of the images, in hyper-
metropic or far-sighted eyes (top row), normal eyes (middle row), and myopic or near-
sighted eyes (bottom row).

A third refractive error to which the human eye is prone is 'astigmatism',
a condition in which the retinal image of a point is not a point but a
line, owing to one of the refracting surfaces (almost always the cornea)
being partly cylindrical as well as spherical in its curvature (Fig. 13).
This results in a blurring of objective lines running in certain directions.
The error is easily corrected, when it is regular as indeed it usually is,
by the appropriate counteracting cylindrical curvature formed on the

28 A TYPICAL VERTEBRATE EYE: THE HUMAN

spectacle lens. As we shall see later, all three of these conditions which
for the human eye are 'errors', are perfectly normal and desirable situ-
ations in the eyes of various vertebrates whose visual requirements differ
greatly from our own.

Fig. 13 — Astigmatism.

a, a square piece of normal cornea whose radius of curvature, r, is the same in all meridians,
images a point p as a point on the screen s. In any other position the screen would intercept
a blur-square.

b, a piece of cornea whose radius of curvature in one direction, /, exceeds its radius of
curvature in another direction, r, is said to be astigmatic. It images a point p as a line
(horizontal in this instance) ih on a screen s placed in its first focal plane, and also as a
line at right angles to the first (the linear vertical image iv) on a screen /' placed in its
second focal plane. The most compact image of p is the 'figure of least confusion', flc, on the
screen /; but this image is a blur-square — the point p is nowhere imaged as a point, as in a.

c, the same piece of astigmatic cornea as in b sharply images the horizontal limbs of a cross
on the screen s, places a blurred cross on the screen /, and sharply images the vertical limbs
of the cross on the screen s". The whole of the objea cannot be sharply imaged at any one
distance from the astigmatic refracting structure.

DIOPTRICS OF THE NORMAL EYE 29

Dioptrics of the Normal Eye — As light enters the eyeball it first
encounters the tissue of the cornea, then in succession the aqueous
humor, the lens, the vitreous humor and the transparent retina on whose
posterior, outer surface the sensory rod and cone cells lie. These trans-
parent structures and substances, exclusive of the retina, are known col-
lectively as the dioptric media. When a light ray comes through the air
into the cornea at one side of the latter's center, it is bent sharply toward
the antero-posterior axis of the eyeball. Upon leaving the cornea and
entering the aqueous humor, the ray is bent again but only very slightly
since the corneal tissue and the aqueous have nearly the same optical
density. The refractive index of the cornea is 1.376, and that of the
aqueous is 1.336, which is about the same as that of water.

Now upon entering the lens, the ray is bent further, again toward the
axis of the eye. The index of refraction of the lens can be taken as 1.42.
Actually, the values for the lens are 1.406 at the center, 1.386 at the
surface, but because of its zoned structure the lens behaves as would a
homogenous body whose index was actually higher than that of any part
of the lens. This figure, 1.42, for the effective index of the lens, does
not exceed the index of the aqueous (1.336) by as much as the latter
value exceeds the index of air (l.OO). This, together with the fact that
the anterior surface of the lens is not as sharply curved as the cornea,
is responsible for the fact — often overlooked — that the cornea does most
of the job of placing the image on the retina. In the optically normal
eye the lens acts like the fine adjustment of a microscope — it adjusts the
position of the image only in a minor way. Some highly myopic persons,
in fact, see clearly without spectacles after the lens has been removed
because of cataract — with the lens in the eye, they have too much focus-
ing power, the focal length of the cornea alone being equal to the
length of their abnormally elongated eyeballs.

Upon travelling through the posterior surface of the lens into the
vitreous humor, our light ray for the first time passes from a medium
of higher density into one of lower density — the vitreous having the
same index as the aqueous. If it were passing through a convex surface,
it would be bent away from the axis of the eye; but since it is here
travelling through a concave surface it is still further converged toward
the axis. In fact, since both surfaces of the lens are in contact with media
whose refractive indices are the same, and the posterior surface of the
lens is more sharply curved than the anterior, the posterior face is the
more important of the two in the static refraction of the eye.

30 A TYPICAL VERTEBRATE EYE: THE HUMAN

The ray now travels to the retina, having crossed the optic axis of the
eye so that it strikes the retina on the opposite side of the axis to the
one on which it entered the cornea. The retinal image of an object is
consequently inverted and much smaller than the object, as is true of
the image of any simple convex lens, as we have seen. The refractive
index of the human retinal tissue, which in life is optically empty, is not
known; but it may be of considerable importance in connection with the
physiology of the fovea (Chapter 8, Section C) . There are indications
that it is higher than that of the vitreous and may approach that of the lens.

It should be borne in mind that it is the difference in refractive index
on the two sides of a boundary surface which, together with the sharp-
ness of curvature of that surface and the direction of curvature (whether
convex or concave), determines the extent of convergence or divergence
of light rays passing through it. The absolute values of the refractive
indices are of no consequence. Hence since the anterior surface of the
cornea is an interface between two very different media (air and tissue)
it is the most important refractive surface in the dioptric media. The
posterior surface of the lens is next in importance, the anterior surface
of the lens least effective (when the eye is not accommodating), and
the posterior surface of the cornea can be ignored entirely.

It is the anterior surface of the lens, however, which in the human eye
is alone modified in curvature in the act of accommodation — hence for
this process, that surface is of paramount importance. We are now pre-
pared to examine the mechanism by which human accommodation is
accomplished.

Accommodation — In the first place the reason for accommodation,
and the extent of the process, need to be clearly understood. The curva-
tures of the refractive surfaces of the ideal human eye and the refractive
indices of ordinary air and of the dioptric media are such that when the
eye is at rest — that is, exercising no muscular effort to accommodate
for nearby objects — objects at the horizon are in focus upon the
back surface of the transparent retina. The seeing-cells, the rods and
cones, stand on this surface like the bristles of a brush. Their length is
appreciable, and since a light ray which helps to form the image strikes
the retina perpendicular to its surface and thus passes axially through a
visual cell, it follows that the optical image may lie anywhere along the
length of the visual elements and still form the same photochemical
image, and be as sharply 'seen' in the form of a cerebral or mental image.

ACCOMMODATION

31

There is thus a certain leeway which the focus of the optical image
may have without its becoming blurred in the consciousness. This lee-
way is in fact so great that without any change in the dioptric structures
of the eye, an object can approach from the horizon to a distance of
about twenty feet* without its image moving back far enough to get out
of the visual-cell layer and into the insensitive chorioid. The image in
the eye is so very small compared with the object that since the move-
ment of the image, either laterally or forward and backward, is minified
to a high degree, the movements of the image over the surface of the
retina (especially through its thickness) are almost microscopic. Conse-

Fig. 14 — The mechanism of human accommodation.

The left half of the diagram shows the structures in relaxation. The thickness of the lens
capsule has been exaggerated one hundred times to bring out its local variations. On the
right, accommodation; by reference to the angular scales, the movements of the various parts
can be discerned. Note that the contraction of both the radial and circumferential portions
of the ciliary muscle has stretched forward the smooth orbicular region of the ciliary body
(to which most of the zonule fibers attach) and has bunched up the coronal region (bearing
the ciliary processes, whose profiles are indicated by the dotted lines). The relaxation of the
zonule fibers has permitted the elastic lens capsule to mold a bulge of sharpened curvature
on the anterior surface of the lens. Note also that the sphinrter muscle of the iris has
contracted, closing down the pupil in its 'accommodation reflex'.

quently, the object may recede from twenty feet to infinity without its
image coming forward more than the length of the rods and cones —
a small fraction of a millimeter (see Fig. 19, p. 43).

Within twenty feet, however, the refracting power of the media must
somehow be increased to keep the image in the visual-cell layer of the
retina. In the human, the anterior surface of the lens is sharpened in

*It is really a bit more, but so variable that for the didactic purposes of this book, twenty
feet is arbitrarily taken as standard.

32 A TYPICAL VERTEBRATE EYE: THE HUMAN

curvature to accomplish this (Fig. 14), and the structures most involved
are the lens capsule, the zonule fibers, and the muscle cells in the ciliary
body. The latter must contract to focus the eye for nearby objects, relax
partially for more distant objects up to twenty feet away, and relax com-
pletely for objects beyond twenty feet. This is why it is restful to the
eyes to gaze out of a window at distant objects for a few moments
occasionally, when doing close work of any kind.

The ciliary muscle fibers are formed into two muscles which blend
with each other and are really only one, since one mass of fibers is de-
rived from the other in the embryo and the two masses have a common
nerve supply and act together, having the same effect upon accommo-
dation in spite of their great difference in orientation within the ciliary
body.

The 'radial' or 'meridional' fibers, as seen in a sagittal section of the
eye, are arranged fanwise, the small end of the mass being fastened
at the scleral roll and the other end being frayed out and distributed
along the whole ciliary body, most of the fibers ending along its inner
surface (Fig. 3; Fig. 5, mb). When this radial muscle (of Briicke) con-
tracts, the effect is a stretching of the flat orbiculus region of the ciliary
body so that its anterior border moves forward — the ora terminalis being
fixed. The corona ciliaris, that portion of the ciliary body bearing the
ciliary processes, is telescoped, its posterior border moving forward but its
anterior attachment at the iris angle remaining fixed. The result of this
forward movement of the region of junction between corona and orb-
iculus is a relaxation of the taut guy-wires of the lens, the zonule fibers.
These are normally in a state of considerable tension when the ciliary
muscle is not contracted; for, as the eyeball grows, before and after
birth, its diameter increases proportionately faster than that of the lens.
Hence the suspensory-ligament fibers, once they have grown out from
the ciliary epithelium and attained connection with the young lens cap-
sule, are placed under constantly increasing lengthwise stress which is
not entirely removed by any compensatory increase in length on their
part. This brings about a slow broadening and flattening of the growing
lens and a permanent state of tension in the suspensory ligament, which
can be relieved only by the contraction of the ciliary muscle.

A portion of the ciliary muscle fibers, the number being often greater
in far-sighted eyes and less in near-sighted ones (where they may even
be entirely lacking) are organized into a ring-like muscle (of Mixller),
analogous to the sphincter pupillae. Although the fibers in Miiller's muscle

ACCOMMODATION 33

(Fig. 5, mm) are thus at right angles to those of the radial (Briicke's)
muscle, the two muscle masses are in no way antagonistic in their action
as are the sphincter and dilatator pupillae. The contraction of Miiller's
muscle heaves the ciliary processes inward toward the axis of the eyeball
and thus substantially supplements the action of Briicke's muscle in
letting up the tension in the zonule fibers. In fact, the muscle of Miiller
is much the more efficient of the two, since no component of its direction
of contraction is wasted in uselessly pulling any part of the ciliary body
forward in the eye. It is only the inward component of the action of the
diagonally-placed Briicke's muscle which is very useful. It is significant
that in far-sighted (hypermetropic) eyes, which must constantly make
extra accommodatory effort (Fig. 12), it is Miiller's muscle — not
Brucke's — which becomes hypertrophied if spectacles are not worn.

To understand what happens to the lens when the zonule is relaxed,
we must recall the nature of the lens capsule and consider its structure
in a little more detail. The capsule is a firm, elastic membrane. If a
cut is made in it, the edges of the cut will tend to roll outward — thus
it is clear that the capsule is normally exerting pressure on the lens
fibers. If the capsule were equally thick throughout and the lens fibers
were plastic enough, the elasticity of the capsule would tend to mold
the lens into a ball if the flattening effect of the tensed zonule fibers
were to be eliminated by cutting them.

Actually, however, the capsule varies greatly in thickness in different
parts and consequently varies locally in the force which its elasticity can
exert upon the lens capsule (Fig. 14). Fincham, who has revised and
modernized the F^elmholtz theory of human accommodation, has care-
fully studied the properties of the capsule and of the decapsulated lens.
Without its capsule, the body of the lens slowly takes on the flattened
form characteristic of the intact lens in situ in the resting eye. Hence
the bulged form of the lens in accommodation is brought about by the
capsule's assertion, upon it, of a molding force more than strong enough
to overcome the tendency of the lens body to flatten. Cutting the zonule
fibers allows the capsule to mold the lens into the same shape it has in
accommodation. The relaxation of the ciliary muscle allows the tensed
zonule fibers to effect a 'physiological decapsulation' of the lens, by pulling
so hard upon the equator of the capsule that the latter 's elasticity is ren-
dered ineffectual, and the lens body assumes the same flattened form
which it takes when removed from its capsule. The contraction of the
ciliary muscle, on the other hand, eliminates the pull of the zonule fibers

34 A TYPICAL VERTEBRATE EYE: THE HUMAN

just as if the latter had been severed and the lens entirely isolated. We
may express these antagonisms and cooperations as a series of equations :

Lens - capsule = lens in situ + relaxed ciliary muscles (no accom.) ;

Lens + capsule - zonule = lens in situ + contracted ciliary muscles;

Lens + capsule - accommodation = lens - capsule;

Lens + capsule + zonule + accommodation = lens + capsule — zonule;
and so on.

The thinnest portion of the lens capsule is a large central area of its
posterior part. This is surrounded by a greatly thickened band which
lies fairly close to the equator. The equatorial region itself is again thin.
On the anterior surface is another thickened zone which lies a little
farther from the equator than the posterior thickening and leaves a
smaller thin central area than occurs on the posterior capsule. This
central thin area of the anterior capsule is also slightly thicker than the
posterior central thin area (Fig. 14).

Ordinarily all of the light used for vision passes only through the
anterior and posterior central thinnings of the capsule — the pupil does
not dilate widely enough to expose the periphery of the lens to incoming
light. The posterior surface of the lens fits the vitreous body so closely,
with incompressible fluid in the retrolental space between the two, that
it cannot change its curvature materially during accommodation. The
anterior leaf of the zonule is probably relaxed more completely than the
weaker posterior leaf at a given stage of accommodation, and the net
result is that only the anterior lens surface is free to deform when the
zonule is relaxed by the contraction of the ciUary muscles. The anterior
zone of thickening in the capsule then proceeds to reduce its diameter
and is stiff enough to force the thin central area of the capsule to form
a bulge, into which the body of the lens is molded. This sharpening of
the curvature of the useful portion of the anterior lens surface increases
the refracting power of the eye and holds the image forward on the
retina in spite of the approach of the object within the 'commencement
point' of accommodation — that is, within the critical twenty-foot distance.

The amount of accommodation which is being exerted at any one
time, and the total amount of which the individual is capable, can be
conveniently expressed in the same units used for designating the focus-
ing power of a lens. The unit in question — the diopter — is not really a
unit at all, for it has a sliding value. The strength of a lens in diopters
is the reciprocal of its focal length in meters. That is, a one-diopter lens
focuses parallel rays at a point one meter away, and a two-diopter lens

ACCOMMODATION 35

focuses at one-half meter, a five diopter lens at one-fifth of a meter, and
so on. The emmetropic eye (Fig. 12, middle row of diagrams) focuses
parallel rays on its receptive layer when it is not accommodating. If now
a one-diopter lens is added, like a spectacle, in front of the relaxed eye,
an object one meter away will be imaged on the retina. A four-diopter
spectacle will enable the non-accommodating eye to image sharply an
object only a quarter of a meter distant. So, we may say that the amount
of accommodation being exerted by an emmetropic eye is four diopters
when, without a spectacle, it images an object at one-fourth of a meter.

-near point at 2

near point at reading distance
^near point at arnn's length
^^^^^^^j-near point at 13'

50 60 70

Age In Years

Fig. 15- — Decrease of human accommodation with age, owing to the progressive hardening
of the body of the lens. Plotted from data of Donders on emmetropic subjects.

By accommodating to a certain extent — four diopters' worth — the focus-
ing power of the crystalline lens has been increased by four diopters over
its strength when at rest; for, this amount of accommodation can take
the place of a four-diopter spectacle placed before the non-accommo-
dating eye.

The range of accommodation — that is, the greatest increase in the
focusing power of the lens — which a person can produce is unfortunately
not a fixed quantity (Fig. 15). Almost as inevitable as death and taxes
is a decrease in that range, with age, to such an extent that the indi-
vidual (unless substantially myopic to begin with) becomes unable to

36 A TYPICAL VERTEBRATE EYE: THE HUMAN

image objects as close as one holds a book to read, and must adopt
spectacles whether he has ever needed them before or not. This phenom-
enon is called presbyopia (literally, old sight), and most of us enter
its realm sometime in our forties. The decrease in accommodating
power is not caused by any weakening of the ciliary muscle, but by a
perfectly normal, progressive hardening of the lens. The ciliary muscle
tries as hard as ever in the presbyopic years — but its force, be it remem-
bered, is not the one which molds the lens. The actual molding force,
the elasticity of the lens capsule, is really quite weak at best, and becomes
wholly inadequate to its task when the body of the lens reaches a certain
stage of firmness. The hardening of the lens is so gradual, however, that
few of us live so long that our graph of the process (Fig. 15) reaches the
line of zero accommodation. When this does happen, the once emme-
tropic eye is still emmetropic — still focuses parallel rays upon its retina;
but its 'near point' (the nearest point at which an object can be sharply
imaged) has moved away from the eye until it is twenty feet away, at the
point where the eye formerly commenced to accommodate for approach-
ing objects.

(C) The Ocular Adnexa

The major anatomical structures which fall under the above heading
are the oculomotor muscles, the lids, and the lacrimal apparatus.

The eyeball lies, cushioned by fat, in a pyramidal cavity in the skull,
the bony orbit. The angle at the apex of the orbit is about 45°, and the
center-lines of the two orbits also make an angle of about 45 . This
brings the mesial walls of the orbits approximately parallel; but for the
axes of the eyeballs to be parallel it is necessary for them to make 22^/2
angles with the axes of the orbits.

The Oculomotor Muscles — Back at the apex of the orbit is the small
aperture by which the optic nerve enters the skull, and close to this
point are the origins of four of the six muscles which rotate the eyeball
(Fig. 16). These are the straight muscles or 'recti'^ — superior, inferior,
medial (internal, nasal) and lateral (external, temporal). They form
the 'muscle cone' around the nerve and diverge toward the equator of
the eyeball. Here they pass through the connective-tissue capsule (of
Tenon) which forms a jacket over the sclera, loosely connected to the
episcleral tissue, and which is a portion of an elaborate system of con-
nective-tissue membranes or fascia in the orbit, one of whose fortunate

THE OCULOMOTOR MUSCLES 37

functions is to bar conjunctival infections from the orbit where they
might do great damage to the eye and the brain.

Becoming tendinous on passing through Tenon's capsule, the inser-
tions of the muscles fuse with the tissue of the sclera. Since the fascial
sheaths of the muscles are continuous with Tenon's capsule, it is possible
to dissect a diseased eye out of the capsule, and by sewing a ball into
the latter, provide a stump for an artificial eye which will move in har-
mony with the good eye of the other side.

Fig. 16 — Oculomotor muscles of man, as seen from above in a dissected head.

On the left, a portion of the superior oblique has been cut away to reveal the inferior
oblique; on the right, the superior rectus has been removed to permit a view of the inferior
rectus. Modified from Adler.

io- inferior oblique; ir- inferior rectus; /r- lateral (external) reaus; mr- medial (internal)
rectus; n- optic nerve; p- pulley through which tendon of superior oblique passes; so- tendin-
ous portion of superior oblique; sr- superior rectus.

Two Other muscles (Figs. 16 and 17) meet the superior and inferior
surfaces of the eyeball obliquely from the nasal side of the anterior part
of the orbit, where one of them, the 'inferior oblique' muscle, is attached.
The other, 'superior oblique', has however greatly lengthened phylogen-
etically and its origin has moved back toward that of the recti. Its side-
wise attack upon the eyeball was preserved throughout the backward
migration of its origin by the development of a tough ring or pulley,
through which it passes. The pulley formed at the old sub-mammalian
site of attachment of the muscle on the anterior nasal orbital wall. As
an anomaly, the muscle may atavistically end here, or a normal superior

38 A TYPICAL VERTEBRATE EYE: THE HUMAN

oblique may be accompanied between the eyeball and the pulley by an
extra muscular slip which has a common insertion with it upon the eye-
ball. An additional and interesting atavism in an occasional human is a
'retractor bulbi' muscle, which in other mammals serves to hold the eye-
ball tightly back in the orbit regardless of the relaxations and contrac-
tions of the eye-rotating muscles. It ordinarily has four parts in mammals,
alternating with the recti and originating with them at the apex of the
orbit. The anomalous human retractor bulbi may exhibit this complete
arrangement. The two oblique muscles, approaching the eyeball from the
nasal side, might seem to give the muscular apparatus extra power for
converging the two eyes — convergent movements being more frequent
than any others — but since they do not pass in front of the center of
rotation of the eye, their chief actions are to tilt the eyeball upward and
downward. Their original purpose was, however, very different (p. 303).
The six normal muscles are supplied by three different cranial nerves,
one of which cares for four of them. Their bilaterally cooperative actions
and the elaborate central-nervous control thereof are beyond the scope
of this elementary description.

The Lids — The eyelids are essentially folds of skin, which were devel-
oped by land animals primarily for cleaning and moistening the cornea,
and which incidentally protect the eye from small foreign objects such
as insects, wind-blown sand, and the like. The cornea of an aquatic
animal is kept clean and succulent by the water itself, through which
no natural particle can travel with sufficient velocity to injure or embed
in the cornea. It is a mistake to suppose that the chief purpose of the
lids is to protect the eye — from blows, and so on; for they are no real
protection against such insults. That function, in man, is taken care of
by the supraorbital ridges of the skull which overhang the orbits and
bear the eyebrows, whose purpose appears to be to divert sweat from
the eyes.

The opening between the lids, which reveals a portion of the eyeball,
is the 'palpebral fissure'. Its temporal and nasal angles are respectively
the (sharper) outer and (broader) inner 'canthi'. In the inner canthus
can be seen the plica semilunaris, a crescentic fold of conjunctiva which
is a vestige of a third, sidewise-sweeping eyelid present in many animals,
the nictitating membrane. Neither the special muscles nor the special
gland (Harder's) of the third eyelid are present, even as vestiges, in
man. Overlying the base of the plica is a pink mass, the caruncle, which
is really a bit of the margin of the lower lid which becomes isolated

THE LIDS

39

• r C S " « S-2

-c 2 ^ v2i c c a,
i2 0-5 i.£-§ a3

M-5-

> 'C '

40 A TYPICAL VERTEBRATE EYE: THE HUMAN

therefrom in the embryo and sometimes bears eyelashes and their assoc-
iated glands as evidence of its true nature.

Near the inner canthus on each Ud margin is a pore raised on an
eminence. These 'punctae lacrimaha' are exits for the tear fluid which
accumulates in a pool, the lacus lacrimalis, at the inner canthus.

The human upper lid (Fig. 18) does most of the work in closing the
eye, though in most vertebrates it is the lower which moves the more.
A continuous sphincter muscle surrounds the palpebral fissure and is
much flattened and very broad where it courses through the two lids
between their outer dermal and inner conjunctival surfaces. The oppo-
nents of this 'orbicularis oculi' muscle are thin muscles running down
into the upper lid and up into the lower. The more important of these
is the levator muscle of the upper lid, which works with the superior
rectus of which it is a derivative. Thus, when the eyeball is turned up-
ward the lid automatically rises. When the levator is paralyzed, as
sometimes occurs in diseases of the nervous system, the individual has
a sleepy look owing to the unsightly drooping of the lid; but the oph-
thalmic surgeon cleverly corrects this by fastening the inside of the lid
to the superior rectus itself.

Between the muscle-sheets of the lids and their conjunctival linings
lie firm plates, one in each lid — the tarsi. Each tarsus is composed of
dense connective tissue and is curved to fit the surface of the eyeball.
Their presence insures a smooth sliding of the lids and obviates any
tendency of the latter to roll up when in action. Embedded in each
tarsus is a row of elongated (Meibomian) glands which open by a series
of apertures behind the lid margin. They represent an additional row of
eyelashes which have disappeared in evolution, leaving their glands
behind them. The sebaceous secretion of these, together with that of
smaller glands (of Zeis) associated with the lashes which are scattered
along the edges of the lids, maintains a film of oily emulsion over the
layer of tear fluid and holds the latter firmly and smoothly against the
eyeball. The tears can spill over onto the cheeks only when they so
accumulate that their weight breaks the retaining film.

The periodic blinking of the lids is ordinarily involuntary and un-
conscious. The rate of blinking varies, but each blink occupies %o of a
second. Its chief values are in moistening and cleaning the cornea and
in pumping the tear fluid out of the lacus lacrimalis — though this is an
incidental function of the lid muscles rather than of the lids themselves.
One might expect the drying of the cornea to initiate the blinking reflex,

THE LACRIMAL SYSTEM 41

but numerous experiments have shown that this is not the case. Though
many factors have been tested for their effect or lack of effect upon the
acceleration or inhibition of the rhythmical blinking of the lids, the im-
mediate cause of it remains quite unknown.

The Lacrimal System — The tear fluid, which can be thought of as
the land animal's substitute for an ocean, is produced continuously in
small amounts (less than 1 cc. per day in the absence of irritation) by
the lacrimal gland. This compound tubular gland lies against the su-
perior temporal quadrant of the eyeball in the anterior part of the orbit,
propped forward by the orbital fat (Fig. 17). Its dozen ducts open
mostly far up under the upper lid. Like the lids themselves, the entire
lacrimal apparatus is lacking in fishes, where it is not needed, and is
much reduced in those aquatic forms which have had terrestrial ancestry.
The tears are mixed with mucus secreted by scattered cells in the con-
junctiva, and most of this fluid is disposed of by evaporation. Any
excess, upon irritation of the eye or in mild emotional states, drains
through the two punctae — chiefly the lower — into a pair of canaliculi
which converge and enter the 'lacrimal sac'. This is a dilatation of the
upper end of the lacrimal duct, a membranous canal which runs vertically
downward, through the bony substance of the skull, to empty into the
nasal cavity. This connection leads to our being able to taste the salty
tears in the back of the mouth when we weep. There are a number of
so-called valves in the tear-drainage system, and its action is rather com-
plicated; but the essential factor in emptying the lacus is a pumping
action by the orbicularis oculi upon the adjacent lacrimal sac. This
makes it possible to conceal emotion and sometimes to forestall weeping
(the spilling of excessive tear fluid onto the cheeks) by rapid blinking.
The primary use of the tears is to clean and wet the cornea. Their
overproduction upon irritation is often entirely effective in washing away
the source of irritation. The fluid contains enough sugar and protein
to be of value in the nutrition of the corneal epithelium, which is able
to absorb proteins. There is some evidence that it is the sole source of
that nutrition. Moreover, the tears are bactericidal to a not unimportant
extent due to the presence in them of a special antiseptic ferment, 'lyso-
zyme'. The most conspicuous thing about the lacrimal system, however,
— psychical (emotional) weeping — is strictly peculiar to the human
animal and to some species of bears, and serves no physiological pur-
pose whatever. It§ value is wholly psychological and economic — as every
woman knows!

Chapter 3

THE VERTEBRATE RETINA

(A) Histology and Physiology

The sensory retina of any vertebrate consists essentially of four layers
of cells. One of these, the pigment epithelium, is not immediately con-
cerned with the process of photoreception. The other three layers com-
prise the retina proper, which lies against the pigment epithelium but is
rarely connected with the latter by any continuity of material.

The Pigment Epithelium — The pigment epithelium of the retina
(Fig. 19) is firmly joined to the inner surface of the chorioid coat.
Each cell in the epithelium is like a six-sided tile and the cells are set
in a regular mosaic with only a thin layer of cement between their
contiguous sides. The base of the cell, toward the chorioid, is also
covered by cement which the cell secretes, so that an unbroken layer
of this cement lies between the pigment epithelium and the chorioid.
The innermost layer of the chorioid is an extremely thin elastic sheet
which, together with the cuticular cement layer between it and the bodies
of the pigment cells, comprises the 'glass membrane' (lamina vitrea).
The whole of the thickness of this really double membrane is often
assigned to the chorioid — or, by some, even to the pigment epithelium,
which clings much more tightly to the chorioid than to the retina proper
when an attempt is made to peel the layers of the eyeball wall apart.
The pigment epithelium belongs to the retina physiologically and embry-
ologically, however, if not anatomically. It is nowhere continuous with
the chorioid, whereas, as we have seen (see Fig. 7g, p. 15) it is contin-
uous at the pupil margin with the anterior prolongation of the sensory
retina.

The free surface of the pigment cell usually bears a number of pro-
cesses which may be few and heavy (even single) or numerous and
filamentous, like a tuft of microscopic hairs (Fig. 20). The granules of
pigment, which consist of a colorless matrix impregnated with a light
brown form of melanin called 'fuscin', are of two sorts — round ones
tending to occupy the cuboidal base of the cell around the nucleus, and
spindle-shaped ones filling the processes and often migrating in and out

42

THE PIGMENT EPITHELIUM

43

of the latter in bright and dim Hght. Pigment may be entirely lacking
over a large area of the epithelium where this lies against an especially
modified area of chorioid (Chapter 9, section D).

* lamina vllrea
** pigment epithelium

receptor layei

'" >c»>v^ "^^m." ^-extllmrmem^.^
^ '^^J^ outernuclear

•^^'i^- ^'\'^"

X'-^-lJ' \ outer plexi-
!*?V rr *^ ^1 form layer

'i^^c\^^'^li T

^r«4^ ^^^■^m.'nner nuclear

inner plexi-
form layer

L^

) ganglion layer ^

nerve fibers

■^'iRtrllmrmemb:

Fig. 19 — The human retina.

At the left, a vertical seaion through the retina in the nasal fundus, as it appears in ordin-
ary histological preparations (fixation in Kolmer's fluid; nitrocellulose embedding; Mallory's
triple stain, Heidenhain's hematoxylin and phloxine). x 500. (Note cross-section of capillary
in inner nuclear layer).

At the right, a 'wiring diagram' of the retina showing examples of its principal elements,
as revealed in material impregnated with silver by the methods of Golgi. Based largely upon
the work of Polyak.

a- amacrine cell (diffuse type); b,b- bipolar cells (ordinary, 'midget' type); c,c- cones;
cb- 'centrifugal' bipolar, believed by Polyak to conduct outward through the retina rather
than inward; db- diffuse bipolar, connecting with many visual cells — chiefly rods; g, g-
ganglion cells (ordinary, 'midget' type); h- horizontal cell — its dendrites connecting only
with cones and its axon with both rods and cones at some distance from the cell-body;
m- Miiller fiber — its ends forming the limiting membranes and its substance serving to
insulate the nervous elements from each other except at synapses; pg- 'parasol' ganglion
cell (one of several giant types, conneaing with many bipolars) ; r, r- rods.

THE VERTEBRATE RETINA

Anterior to the ora terminalis the pigment epithelium passes over the
cihary body as the outermost of the two layers of the ciliary epithelium
and is almost unchanged except for an increase in the height of its
cells and the disappearance of all processes together with the spindle
form of pigment granule. Its continuation on the back of the iris is

Fig. 20 — Pigment-epithelial cells, x 500.

The horizontal line beneath each drawing shows the position of the external limiting mem-
brane. A portion of the lamina vitrea is shown as a heavy black line. Spaces occupied by
cones are marked c; those filled by rods are marked r.

a, group of cells from an unstained, flat mount of human pigment epithelium, as seen from
the chorioid side. Through the clearings formed by the nuclei, some of the elongated pig-
ment granules in the distal part of the cell can be seen.

b, two human pigment cells from the nasal periphery, in vertical sertion. One cell is opposite
a cone, and bears a delicate tubular process which ensheathes the cone outer segment {cf.
Fig. 19). The other cell is opposite only rods, and is devoid of processes.

c, pigment cell of a mouse opossum, Marmosa mexicana, showing the paucity of retinal
pigment charaaeristic of many strongly nocturnal animals.

d, pigment cell of an African lungfish, Protopterus eethiopicus, showing a mass of fila-
mentous pigment-laden processes markedly differentiated from the body of the cell.

e, pigment cell of goldfish, Carassius auratus, light-adapted. The two or three heavy proc-
esses contain relatively little migratory pigment (in rod-like granules) in their tips {cf. Fig.
62, p. 146; Fig. 94, p. 237).

almost devoid of pigment in those animals in which it has produced
a dilatator pupillas (Fig. 7, p. 15). At the edge of the pupil the layer of
cells doubles back upon itself and continues, now heavily pigmented, to
the periphery of the iris as the latter's most posterior layer of tissue.
There its pigmentation disappears and a clear epithelium proceeds over

THE VISUAL CELL-LAYER 45

the ciliary body, as the innemiost of the two layers of the ciliary epi-
thelium, to the ora terminalis. At this point the simple epithelium sud-
denly becomes stratified and complex to form the sensory retina.

Travelling thus forward to the pupil in the pigment epithelium and
backward again into the sensory retina proper, we are easily able to see
that the entire retinal coat of the eye reaches to the pupil margin and
forms a two-layered cup. The two major layers — pigment epithelium
and retina proper — develop directly from the two layers of the embry-
onic optic cup, which arises as a bubble of tissue on the side of the
brain, becoming constricted off therefrom and deeply indented on the
side toward the skin. This indentation gives the vesicle an outer and an
inner layer and an opening, aimed toward the surface of the head, into
which the lens is received after its separation from the skin (see Fig. 38,
p. 106). Thereafter the opening becomes (relatively) smaller, and per-
sists as the pupil.

The Visual-Cell Ltayer— Standing on the external surface of the
retina proper, and constituting its receptive layer, are the rods and cones
(Fig. 19). These elongated cells thus point away from the light, which
must pass through the remainder of the retina to reach them (hence the
complete transparency of this tissue as contrasted with the brain, which
has a similar histological organization). Their tips are pressed against
the pigment cells or are even buried in deep indentations in them, or
between their processes when such are present. The processes in turn
may reach nearly to the bases of the rods and cones so that they are
deeply interdigitated with the latter. Though there is seldom a conti-
nuity of substance, the dovetailing of the sets of processes and visual
cells is so intimate and firm that one or the other is often torn in two
if the retina and chorioid are forcibly separated. In other cases the
absence of all pigment-cell processes may make a separation very easy,
and only the optic nerve, the fusion of the two layers of the optic cup
at the ora terminalis, and the pressure of the vitreous then hold the
retina firmly and smoothly in place.

At the level of the bases of the rods and cones the retina has its ex-
ternal limiting membrane (briefly, the 'limitans') which may be likened
to a piece of wire screening through each hole of which a rod or cone
projects. The visual cells are a tight fit for the holes and are thus kept
perpendicular to the membrane and prevented from getting out of line
by any sliding lengthwise past each other. In some retinas, delicate hair-
like processes from the outer surface of the membrane itself form so-

46 THE VERTEBRATE RETINA

called fiber-baskets, fused with the surfaces of the bases of the visual
ceils and anchoring them very firmly in place.

On the inner side of the limitans lie the nuclei of the rods and cones.
The diameters of these are ordinarily much greater than those of the
cytoplasmic parts which protrude outward through the limitans. This
results in the nuclei piling up into several rows (forming the 'outer
nuclear layer') the number of which in a given retina will be roughly
equal to the quotient of the square of the diameter of the nucleus divided
by the square of the diameter of the predominant type of visual cell.
Cones are usually so plump at their bases that there is room for their
nuclei to lie up against the limitans or even above it; but a rod nucleus
may lie far below its rod, being connected with the latter by a slender
thread which winds its way up among the intervening rows of nuclei.

The Bipolar Layer — From each visual-cell nucleus a short thread-like
*foot-piece' travels inward (toward the vitreous) until it clears the other
visual-cell nuclei, and then expands into a terminus which may be either
smoothly rounded, or branched like a bird's foot (Figs. 19, 22, 23, 24).
This is related, as in a handclasp, to a similar arborization at the outer
end of a 'bipolar' neuron, whose cell body lies deeper in the retina
toward the vitreous. A bipolar dendrite may embrace several or a great
many visual-cell termini, so that the number of bipolar cells in a retina
is always less than the number of visual cells. The branched process of
the bipolar cell which joins to the visual cells, and the similar process
from the bipolar cell-body which travels in the opposite direction (to-
ward the vitreous) are however much more slender than the cell-body.
The bipolar nuclei are consequently piled up in several layers like those
of the visual cells, and this second band of nuclei forms the 'inner nu-
clear layer' of the retina (Fig. 19). In this layer, along with the nuclei
of bipolar cells, are a (usually) smaller number of nuclei belonging to
several types of cells which will be mentioned later.

Some of the bipolar cells each connect with but one cone. Such are
the numerous 'midget bipolars' of the primate retina (Fig, 19, b). Other,
'diffuse' bipolars (Fig. 19, db) of several types may each embrace a great
number of rods, and some cones as well. In many retinae there are diffuse
bipolars which connect only with rods, or only with cones; but such
elements appear to be lacking in man.

The inner nuclear layer is separated from the outer nuclear layer by
a feltwork of the delicate nerve fibers which make the connections

BIPOLAR AND GANGLION LAYERS 47

between visual cells and bipolars. This is the 'outer plexiform layer'.
An 'inner plexiform layer' also occurs on the vitread side of the inner
nuclear layer, and has a similar significance. In it lie the synaptic junc-
tions between bipolar cells and the innermost of the three masses of cells
concerned with the projection of the image to the brain — the 'ganglion
layer'.

The Ganglion Layer — The cells of this layer (Fig. 19) have either
small or large bodies and simple or elaborate dendrites which reach up
into the inner plexiform layer to meet the termini of the bipolars. Each
ganglion cell gives off a slender axon process which courses along the
inner surface of the retina, next to the vitreous. All of these fibers, from

Fig. 21 — The optic chiasma.

a, of man, showing partial decussation of optic nerve fibers.

b, of bird, showing total decussation; in some vertebrates (i.e., most fishes) the nerves are
not thus plaited — but whether the fibers are interwoven or not, they all decussate in non-

mammals.

c- chiasma; n- optic nerve;

retina; /- optic tract, which enters brain.

all over the sensory retina, converge at one place in the 'fundus' (back)
of the eye and there turn parallel to each other and pass outward
through the retina, chorioid and sclera in a compact bundle as the optic
nerve, which travels toward the brain (Fig. 21).

A ganglion cell may gather in the axons of several bipolars (Fig. 19,
pg) , just as one of the latter in turn often connects not with one visual
cell but with several. This has been called the 'inward convergence' of
the visual cells upon optic nerve fibers, or 'summation'. The impulses
which travel down several visual-cell foot-pieces are summated in their
efforts to stimulate a single bipolar cell, and numbers of bipolar nerve-
impulses are in turn gathered into single ganglion cells and optic nerve

48 THE VERTEBRATE RETINA

fibers. This phenomenon of summation is of the utmost importance in
the physiology of the retina, and will be discussed again when certain
other concepts have been introduced.

The three kinds of retinal elements so far mentioned — visual, bipolar,
and ganglion cells — are those concerned in the simple, straightforward,
projective pathway of the visual impulse to the brain. There are four
other types of cells which remain to be described: Miiller fibers, neu-
roglial cells, horizontal cells, and amacrine cells.

Miiller Fibers — Miiller fibers may be likened to rivets which run
through the whole thickness of the retina proper and bind its layers
together (Fig. 19, m). Their outer ends form the external limitans and
their inner ends are expanded into trumpets or pyramids whose bases,
against the vitreous, are six-sided and are fitted together as an unbroken
mosaic, the internal limiting membrane of the retina. This is not a true,
isolable membrane but simply the inner surface of the retina. The vitre-
ous which touches the internal limitans may be a little tougher than the
rest, like the skin on a cornstarch pudding; but it is still part of the
vitreous — there is no distinct layer at the retino-vitreal interface which be-
longs to neither structure. The retina and vitreous are simply in contact.
The nucleus of a Miiller fiber lies about half-way through the thick-
ness of the inner nuclear layer and is very easily identified by its elon-
gated oval form. The boundary surface of a Miiller fiber, however,
cannot be made out at all unless the cell is isolated by the procedure
of macerating the retina; for the Miiller fibers have irregular expansions
and cavities in them, and occupy a surprising amount of the total volume
of the retina. If we imagine building a model of the retina by using wires
for the nerve fibers in it, and large glass beads for their nuclei, we could
then represent the whole population of Miiller fibers best by filling in all
the empty space with wax or some such substance. All of the nuclei in
the retina sit in pockets in the Miiller fibers, which at the levels of the
nuclear layers form a sort of sponge-work. Every nerve-fiber is likewise
insulated from every other by a film of intervening Miiller-fiber sub-
stance; and only at the synaptic handclasps between nerve-fiber ends is
there opportunity for separate nerve cells actually to come in direct con-
tact.

Neuroglia — The neuroglial cells of the retina are small and not num-
erous. They are like one of the chief types of glial elements in the brain
and spinal cord. While glial cells are abundant and im.portant in serving

SUSTENTATIVE AND INTEGRATIVE CELLS 49

as the connective-tissue of the central nervous system, their place is taken
in the retina by the Miiller fibers, which do the same job even better and
other jobs in addition. We may fairly consider the glial cells of the
retina to be meaningless, and present only because of their inheritance
from the brain wall of which the retina is, after all, a part. Occasionally
they seem to resent their idleness and become altogether too busy, gener-
ating a 'glioma' — a particularly disastrous type of tumor whose presence
calls for the immediate removal of the eye to prevent a fatal involve-
ment of the brain by way of the optic nerve.

Horizontal and Amacrine Cells — Although the Miiller fibers and
neuroglial cells are certainly not impulse-conducting elements, the 'hori-
zontal cells' are under suspicion of performing some sort of integration
of the retina. If we think of the visual^bipolar->ganglion-cell chain as
running vertically through the retina, then the amacrines and horizontal
cells do their work in a horizontal direction. The horizontals have their
cell-bodies among those at the outer surface of the inner nuclear layer
(Fig. 19, h). In lower vertebrates the horizontal cells are chunky and
epithelioid, or ropy and anucleate, and seem only to have a supporting
function like the Miiller fibers. In higher vertebrates, however, they more
often have many spider-leg processes running in the outer plexiform
layer. Thus they may give the appearance of nerve cells and very prob-
ably do conduct laterally, tying up one area of the retina with another
just as regions of the cerebral cortex are interconnected by association
fibers. Those of mammals (Fig. 19, h) are certainly conductive, and in
man have their stubby dendrites connected with cones and their long
axons connected with distant rods and cones.

The 'amacrine' cells ordinarily have this same horizontally integrative
function. Their exact action and its effects upon subjective visual phe-
nomena are about the biggest remaining mystery in the physiology of
the retina. Their nuclei tend to lie in the inner half of the inner nuclear
layer and each gives off a single process which passes vitread and then
branches more or less, the branches being short or very long (Fig. 19, a).
The amacrines seem to associate the bipolar^ganglion-cell synapses, per-
forming for the inner plexiform layer the same function that the con-
ductive types of horizontal cells do for the outer.

The action of these two types of cells would appear to be detrimental
to the preservation of the pattern of the retinal image during its 'wire-
photo' transmission to the brain in the form of nerve-impulses. If all the

50 THE VERTEBRATE RETINA

amacrines were carrying impulses at once, the result would certainly be
a hopeless garbling of the projective transmission and a blurring of the
cerebral picture of the external visual field. One would, then, expect to
find amacrines very few or even lacking in the retinae of those animals
whose vision is keenest and whose ability to discriminate fine-detailed
patterns is greatest. Yet it is in just such animals that the amacrines are
most abundant. In the birds, for example, they may even outnumber the
bipolar neurons. Obviously, only a few can be in action at any one time,
and they make of the retina an elaborate switchboard in which now one,
now another conduction may be enhanced or inhibited.

In primates, some of the elements formerly believed to be 'amacrine'
(hterally, 'lacking an axon') have recently been found to possess axons
after all. If their axons and dendrites have indeed been correctly iden-
tified (and the identifications are so far on a purely morphological basis) ,
then such elements are really bipolars of a peculiar sort — they conduct
toward the receptor layer. Such a supposed 'centrifugal' bipolar is shown
in Figure 19 (cb). Their discoverer, Polyak, thinks that they serve to
alter the state of activity of the visual cells. What this may mean, trans-
lated into terms of visual physiology and visual psychology, is not clear.
It seems as likely that the centrifugal bipolars intensify (or prolong) the
activity of ordinary bipolars in a given amount or pattern of illumin-
ation, by (so to say) taking excitation from their lower ends and putting
it back in at their tops. Anyone familiar with radio hook-ups (which the
diagram in Fig. 19 rather resembles!) can see how the centrifugal bipolar
may be compared with a tickler coil in a regenerative circuit.

There are many true amacrines in primates, however; and these axon-
less, horizontal integrators are abundant in other vertebrates — partic-
ularly so, in birds (v. s.).

A moment's thought about the mystery of the amacrines suffices to
convince one that the retina is more than just a sense organ which re-
tails to the brain, parrot-fashion, the physical changes in the environ-
ment. The retina is an association center with every bit as complex a
mode of action as the cerebral cortex itself. The elucidation of its switch-
board activities is almost beyond the realm of physiology.

Nutrition of the Retina — The nervous tissue of the retina probably
does not have a high rate of metabolism, but the rods and cones are very
sensitive to any interference with their supplies of materials and oxygen.
These come from the chorioid, which aside from its light-absorbing func-

NUTRITION OF THE RETINA 51

tion is wholly devoted to the nutrition of the visual cells. The turnover
of substances must be very great, for the chorioid is very rich in blood
vessels which indeed comprise most of its bulk in many animals.

Just outside of the lamina vitrea lies a network composed of broad,
flat capillaries. This 'choriocapillaris' reticulum (Fig. 6b, p. 14) is so fine-
meshed that its capillaries total a greater portion of its area than do
the spaces between them. It is with the blood in the choriocapillaris that
the visual cells make their exchanges of supplies and wastes, liaison
being effected by the pigment epithelium which is thus taking in and
giving off materials at both of its surfaces continuously. The retina
often has blood vessels clinging to or embedded in its inner surface, but
these are usually concerned only with the nutrition of the inner layers
of the retina. Even where (as in most mammals) capillary branches of
these vessels invade the retina itself, they almost never reach outward
beyond the inner nuclear layer and obviously belong only to the vitread
portion of the retina. Such a capillary shows in Figure 19.

The choriocapillaris is supplied with blood by a layer of arteries
outside of it in the chorioid, and drains into a layer of large inter-con-
necting veins which lie on the scleral side of these arteries (Figs. 4a, 6a;
pp. 8, 14). The veins converge in the four quadrants of the eyeball to
pour their contents into the four great 'vorticose veins' which conduct
the blood away from the equator of the eye. Other vessels also penetrate
the sclera anteriorly and supply or drain structures other than the retina.
The vessels mentioned above, which supply the inner layers of the retina,
are few and are branches of vessels which enter the eyeball in or along
with the optic nerve. True retinal vessels are present only in the eels and
the mammals — -and not even in all of the latter, some of whose retinas
(e.g., in the rhinoceros) are as completely avascular as those of the lower
vertebrates.

All of the vessels concerned with the eye apart from the retina— and
even including those last mentioned above — do not, taken together, com-
pare in abundance with the rich chorioidal circulation. This latter exists
solely for the benefit of those cells of the whole eye which are most
important, if any are that: the rod and cone visual cells.

The Optic Nerve — The human optic nerve takes a long, slightly
undulant course to the apex of the orbit and there enters the cranium
(Fig. 16, p. 37). It is flexible, and by its length allows enough slack to let
the eye rotate freely. It contains more than a million nerve fibers, most of

52 THE VERTEBRATE RETINA

which transmit visual impulses, though many are centrifugal. It is heavily
ensheathed by tendinous and vascular coats continuous on the one hand
with the sclera and on the other hand with the meningeal coverings of
the brain, and is divided by internal septa, of connective tissue and neu-
roglia, into many fiber-bundles. The central retinal artery and vein join
the nerve at some distance from the eyeball and run through its center
to emerge within the eye at the nerve head, where they branch over the
inner surface of the retina. The optic 'nerve' is called such only for
convenience. It is not a true nerve but, like the retina, an ectopic portion
of the brain itself.

Within the cranium the two optic nerves cross through each other
and continue, as the 'optic tracts', into the brain. The crossing or
'chiasma' is especially complex in man and in all other mammals, for
in them only some of the fibers from each eye cross into the opposite
optic tract, the others going directly into the tract on the same side.
In other vertebrates, the crossing or 'decussation' of the fibers is com-
plete— that is, all of the fibers from each optic nerve enter the opposite
side of the brain (Fig. 21). No special advantage is gained by such an
arrangement — it arose mysteriously along with the numerous similar
decussations in the tracts of the brain, brain stem, and spinal cord; but
there is a special value of partial decussation which will be found ex-
plained in Chapter 10, section D. Even where the decussation is total,
the chiasma is seldom a simple anatomical crossing of one whole optic
nerve over the other. This is indeed the situation in most fishes; but
elsewhere the two nerves are interwoven to a greater or lesser extent
(Fig. 21b).

(B) Types of Visual Cells

General Types— Rods versus Cones — The visual cells of vertebrates
are of two general types which were long ago given the names 'rod' and
'cone' — though with our superior modern knowledge of their phylogen-
etic ramifications and physiological characteristics we might wish that
a more apt pair of names could be substituted for the traditional ones.
In a given retina containing both highly sensitive visual cells (rods)
and relatively insensitive ones (cones) , the high- and low-threshold cells
can always be told apart; but the rod of one retina may resemble struc-
turally the cone of another, or may give evidence of having been recently

OPTIC NERVE; RODS VS. CONES 53

derived from a cone-type in an ancestor of different habits. In an at-
tempt to resolve the confusion resulting from an overemphasis of shape-
differences — which has even led some to deny any distinction between
rods and cones! — the writer several years ago proposed the names
'photocyte' and 'scotocyte' for the two physiological types of visual
cells contrasted in the Duplicity Theory (see next Section). But it is
perhaps too late to bring about any such revolution in the terminology.

Of the two types, there can be no doubt that the cone is the older and
more primitive. This statement however — which is quite contradictory
to any the reader will find in other books — is not to be taken to mean
that cones entirely like those of man were the original vertebrate visual
cells. It is certain, for instance, that the ancestral cell lacked any means
of analyzing colors. It is equally certain that the common ancestor of
present-day rods and cones lacked any such ingenious sensitizing sub-
stance as rhodopsin (see Chapter 4) . With a slender, pointed, stimulable
organelle, the outer segment, derived from a formerly vibratile flagellum
(see Chapter 5, section B) and connecting directly to a simple afferent
neuron, the pro-vertebrate visual cell could not but have been a high-
threshold receptor, which limited the excursions of its owner to the
brightly lighted surface waters.

Rods came later, as a means of extending the period of activity over
a greater portion of the twenty-four hours. They were derived quite
simply from cones by the enlargement of the outer segment and by an
increase in the number of visual cells connected to each nerve cell. It
was not desirable for all of the visual cells to make these changes, for
unless two types were preserved side by side in a nice balance, sensitivity
to dim light could not be increased without too great a sacrifice of re-
solving power. The needs of the animal — whether greater for sensitivity,
or for visual acuity — then determined the proportion of small un-sum-
mated and larger, summated visual cells which would give him optimal
visual capacity. With the invention of the powerfully sensitizing rhod-
opsin by the rod on the one hand, and the differentiation of a photo-
chemical basis for hue-discrimination in the cones on the other hand,
the widely useful duplex retina as we know it today came into being.

Single Cones — Because of the antiquity and priority of the high-thres-
hold cell, we will consider first the cytology of a typical single cone such
as that of the frog (Fig. 22c). The elaborate cytoplasmic portion of this
complex cell protrudes through a lacuna of the external limiting mem-

54

THE VERTEBRATE RETINA

brane, which constricts its base firmly and keeps the nucleus of the cone
on the vitread side. The tapered photosensitive tip of the cell is the
outer segment, the remainder of the cell down to the nucleus being the
inner segment and representing the columnar body of the ancestral epi-
thelioid ependymal cell. In the distal end of the inner segment lies the

( cf

Fig. 22 — Single cones.

1000.

a, of sturgeon, Acipenser fulvescens. b, of goldfish, Carassius auratus; light-adapted {i.e.,
with myoid contraaed — cj. Fig. 62, p. 146; in fishes, the cone nucleus often lies partly or
wholly above the external limiting membrane, as here), c, of leopard frog, Rana pipiens:
dark-adapted {i.e., with myoid elongated — c/. Fig. 64, p. 148). d, of snapping turtle,
Chelydra serpentina, e, of marsh hawk. Circus hitdsonius; from the circumfoveal eminence,
f, of man; from the circumfoveal eminence.

d- oil-droplet, embedded in: e- ellipsoid; /- foot-piece; /- external limiting membrane;

m- myoid; n- nucleus; o- outer segment; p- paraboloid.

ellipsoid, whose shape in the frog cone happens to justify this geomet-
rical name, though this is seldom true. Embedded distally in the ellipsoid
is the oil-droplet, which in some frog cones contains a dissolved yellow
pigment. The stalk-like portion of the inner segment is highly contrac-
tile (Chapter 7, section B) and hence is called the myoid (= muscle-
like). The myoid joins the large, ovoid nucleus in which the chromatin

SINGLE CONES

55

occurs in a reticulum of many small granules. From the region of the
nucleus a short, thick, dendritic 'cone-foot' proceeds vitread to make a
synapse-like junction with a bipolar dendrite.

&

y/

Fig. 23— Rods. X 1000.

a, generalized rod, showing organelles as they might appear if visible in the living cell;
note myeloidal spiral and centrosomic Fiirst fiber in outer segment, diplosome and Kolmer-
Held fiber proceeding therefrom in inner segment, b, rod of Protopterus cethiopicus—
unusual, in that it contains an oil-droplet, implying secondary origin from a cone (c/. Fig.
25). c, rod of goldfish, Carassius auratus; light-adapted (i.e., with myoid elongated — cf.
Figs. 62 and 63). d, common or 'red' (rhodopsin-containing) rod of leopard frog, Rana
pipiens; dark-adapted {i.e., with myoid contraaed — cj. Fig. 64). e, 'green' (Schwalbe's)
rod of Rana pipiens. i, rod of flying squirrel, Glaucomys v. volans; exemplifies the fila-
mentous type characteristic of many strongly nocturnal animals, g, human rod from near
the temporal side of the macula lutea.

d, oil-droplet; e- ellipsoid; /- foot-piece; /- external limiting membrane; m- myoid (the
corresponding portion of the inner segment is non-contractile in e, f, and g); n- nucleus;
o- outer segment; p- paraboloid.

56 THE VERTEBRATE RETINA

Not all single cones are built like those of the frog. The oil-droplet
is lacking in the cones of nearly all living forms lower than the frogs;
but even so there are reasons for thinking the oil-droplet to be a very
primitive visual-cell feature. Such droplets occur in pigment epithelial
cells, which are homologous with the visual cells, and apparently also
(in salamanders) in the type of brain-cell from which the rods and cones
originated. The ellipsoid, which appears to be a light-concentrating
device, is sometimes supplemented by a second dioptric organelle, the
paraboloid, lying proximal to it in the myoid. The paraboloid may have
some very important function other than its incidental optical one.
While the ellipsoid always stains heavily with acid fuchsin, an out-
standing peculiarity of the paraboloid is its usual refusal to take any
stains at all. It is quite likely that some paraboloids are fluid vacuoles —
perhaps sometimes artificial spaces (Figs. 22a, 23b, 24a and b) ; but
many are solid or semisolid (Figs. 2 2d, 25) and keep their shape when
expressed from the living cell.

The cone outer segment may actually be cylindrical when it is so very
slender that it could hardly be expected to taper, as in many lizards and
birds, and even sometimes when there is plenty of room for a more
bulky, conical structure (Fig. 22). The myoid may be quite non-con-
tractile and thus undeserving of that name, as in man; and it may be
permanently greatly elongated, marooning the body of the cone opposite
or even beyond the tips of the rods (flying squirrels, some lampreys and
snakes — see Fig. 69a, p. 167). The nucleus of the frog cone is typical
structurally, but not as regards its position, for cone nuclei almost always
lie in contact with the limitans or even (some fishes) beyond it, on its
scleral surface (Fig. 22a and b).

One of the most noteworthy peculiarities which cones may have is
that presented by the cones of the greater portion of the human retina,
and also by some other placental mammals, the dog and cat for exam-
ple : the cone outer segment is a cylinder enclosed by a tubular process
of the pigment epithelial cell opposite to it, and apparently (though this
is not yet certain) fused at its tip with the pigment cell, actual proto-
plasmic continuity existing between the two (Figs. 19, 20b; pp. 43, 44).
No such arrangement is ever seen in rods, and its obvious advantages for
the facilitation of the nutrition of the cone constitute important evidence
for the cone's having a faster metabolism than the rod — something
which has long been suspected on other grounds.

RODS; HOMOLOGY WITH CONES 57

Rods — One rod would do about as well as another to illustrate rod
structure, for rods do not differ from retina to retina nearly so much
as do cones. The rod (Fig. 23) has the same principal parts as the cone
— outer and inner segments, nucleus, and foot-piece. The outer segment
is almost without exception a perfect cylinder and the inner segment is
often more slender — sometimes, as in bony fishes, much more so.

The rod in man and other mammals is not contractile; so, the term
'myoid' for the undifferentiated part of the inner segment would be a
misnomer. A structure corresponding in microchemical behavior to the
cone ellipsoid is present, though it is probably optically functionless.
Rod nuclei tend to be smaller, more nearly spherical, and with much
larger and fewer masses of chromatin than cone nuclei. The latter hav-
ing preempted positions against the limitans (the cones being the first
visual cells to differentiate in embryonic retinae), the rod nuclei per-
force contact the limitans only between cone nuclei and for the most
part are forced to pile up below it to form the thick outer nuclear layer.

Cones ordinarily vary considerably in different retinal regions, being
more slender and more numerous toward the fundus. Rods are uniform
in concentration everywhere except as this is influenced by the cones —
it is as though the cones had been distributed in the retina first, and
then the spaces between them neatly filled in with as many rods as
would conveniently fit. Rods are ordinarily uniform in diameter through-
out a retina, but their length tends to increase slightly and slowly from
ora to fundus. The center of concentration of cones, or of rods when
they have such a center, does not necessarily lie anywhere near the optic
axis of the eye. Seen 'on the flat', the rod and cone mosaic exhibits a
pattern which in different animals may have the hexagon, the square,
or some other geometrical figure as its unit. These patterns have not
yet been sufficiently studied for them to yield up any ulterior meaning
which they may have.

Homology of Rods and Cones — Cone and rod are homologous part
for part and have many points in common. The outer segments of both
have thin sheaths filled up with a lipid ground-substance in which one
or more closely wound spiral filaments of another lipid material, derived
from mitochondria, are embedded (Fig. 23a). These show faintly or
clearly in large rod outer segments (Figs. 25 and 26), rarely also in
cones; but they are presumably always present. When too heavily
stained, they commonly give an appearance of transverse discs (Figs.

58 THE VERTEBRATE RETINA

22f, 23g). A long filament runs axially or peripherally in the outer seg-
ment of (again, presumably) every visual cell and, just within the inner
segment, is connected with a pair of granules from which a second,
much shorter, filament proceeds down the inner segment for a way
(Fig. 23 a). This filament-and-granule apparatus, collectively, is the cen-
trosome of the cell, whose function in visual physiology, if any, is not
known. Rods may contain paraboloids, or even oil-droplets (Figs. 23b,
25b, c) , though only when the rods have had a peculiar history (Chapter
7, section D). The rod foot-piece may be just like a cone-foot; but in
animals whose rods are very slender and numerous (teleosts, mammals,
and nocturnal birds) it is a slender filament terminating in a highly
specialized, unbranched 'rod end-knob' — apparently to make more com-
pact the connections of many rods to single bipolars (Fig. 19, p. 43).

It is also in such animals that the rod and cone nuclei are most sharply
differentiated as to size, shape, and chromatin distribution. In forms
with fewer, more bulky rods (lampreys, amphibians, many reptiles) the
rod and cone nuclei are indistinguishable on any basis other than pos-
ition, and the foot-pieces may be nearly or quite identical. In connection
with the question whether the rod or the cone is the more primitive cell,
it is significant that when the nuclei and foot-pieces are alike in a retina,
they both resemble the cone structures of retinae in which they differ —
and, cone-type nuclei are more like nuclei in general than are rod-type
nuclei. The heavy, dendritic cone-foot would also appear to be a more
primitive sort of connecting process than the peculiar rod-fiber and its
end-knob. Where they are markedly differentiated, the differences be-
tween rod and cone nuclei have no relationship to physiological differ-
ences which we are able to discern at present.

Green Rods — There is a type of so-called rod, restricted to the am-
phibians, whose very long stalk is but slightly contractile (Fig. 23 e).
It lacks rhodopsin and this, together with the shortness of its outer
segment, would necessarily make it have a relatively high threshold.
Functionally, this 'green rod' (of Schwalbe) is probably more cone-like
than rod-like — its nucleus even lies in the inner part of the outer nuclear
layer, alongside the cone nuclei; but its origin is quite unknown.

Double Cones — Even more mysterious are the 'double cones' — and
the puzzle they present is particularly irritating to the curious inves-
tigator because they are so very widespread among vertebrates. If they
occurred in only one or two animals, we might dismiss them as a curi-

DOUBLE CONES

59

osity. Perhaps if they occurred in the human retina we would before
now have gained some clue to their role in visual processes; but their
functional significance, their exact mode of formation in the developing
retina, and the probable time and manner of their evolutionary origin
have yet to be determined. Next to the amacrine cells, the double cones

Fig. 24 — Double and twin cones, x 1000.

a, double cone of a holostean fish, the bowfin, Amia calva. b, double cone of leopard
frog, Rana pipiens; dark-adapted {i.e., with myoid of chief cone elongated), c, double
cone of western painted turtle, Chrysemys picta marginata. d, double cone of European
grass snake, Matrix natrix. e, twin cone of a teleost fish, the bluegill, Lepomis m.
macrochirus; light-adapted (i.e., with fused myoids contraaed). f, conjugate element (of
Fundulus heteroditus; after Butcher) characteristic of some teleosts; perhaps intermediate
between a and e, perhaps instead a derivative of e.

c- 'clear mass'; d- oil-droplet; e- ellipsoid of chief cone; e'- ellipsoid of accessory cone;

/- foot-piece; g- 'granular mass'; /- external limiting membrane; m- myoid; n- nucleus of

chief; n- nucleus of accessory; o- outer segment of chief; o'- outer segment of accessory;

p- paraboloid.

are physiologically the most obscure elements in any and all retinae.
They have unfortunately not greatly interested visual physiologists,
since the latter have their attention focused upon the human retina, in
which double cones are lacking.

Double cones appear phylogenetically first in the holostean fishes
(Fig. 24a). They occur in amphibians, reptiles, birds, one monotreme
(Ornithorhynchus) and marsupials, but not in any known placental

60 THE VERTEBRATE RETINA

mammals although some of the most primitive of these may prove to
have them when examined. So, most vertebrate groups have double
cones; yet we have no idea what they mean. The most that can be said
is that the number of double cones, relative to the total number of cones,
tends to be high in strongly diurnal animals and low in strongly noc-
turnal ones. As a maximum, double cones may about equal in number
the single cones of the same retina.

The typical double cone (Fig. 24b, c ) consists of two very unlike
cones fused together in the lower myoid region. One member — the chief
cone — is always very much like the single cones in the same retina. The
other, or accessory cone is decidedly different. The ellipsoid is usually
unclear in outline proximally and its material blends with the ground
substance of the inner segment. There is almost never an oil-droplet,
but an enormous paraboloid is almost invariably present. This so dis-
tends the accessory myoid that the myoid of the chief cone is thinned
and curved around the paraboloid region so as to be almost indistin-
guishable proximally. There are two nuclei, and some indications that
the two foot-pieces connect with different bipolars. The two members
of a double cone seem to supplement each other — an organelle which
one lacks, the other possesses; but since everything that may be present
in the two members together may also occur in one single cone, the
segregation of parts in the double cone is without obvious meaning.

Twin Cones — Quite another sort of element is the 'twin cone' (Fig.
24e) found in so many teleost fishes. In this receptor the two members
are identical and are fused throughout the length of the inner segment.
Thus the twinned myoid contracts and elongates as a unit during photo-
mechanical changes, whereas in double cones only the chief member
moves, the accessory having no myoid in the proper sense of the word.
Twin cones are strictly a teleostean monopoly. These fishes being a
terminal group in evolution, it is impossible to believe that ordinary
double cones developed from twin cones; nor is there much reason to
suppose that twin cones were ever double ones of the type described
above. But there are elements in some teleosts which for want of a third
possible name we shall have to call double cones (Fig. 24f ) . They seem
to represent twin cones in which the two ellipsoids and outer segments
have become unequal in size and different in staining properties and
hence, chemico-physical makeup; but the zone of fusion still extends the
whole length of the inner segment so that the two myoids contract and

TWIN CONES; OPHIDIAN DOUBLE CONES 61

lengthen as one. These structures indicate that the makeup of the com-
mon double cone is worth imitating for some reason; and we shall see
shortly that the snakes have also discovered this for themselves. But,
until the distribution of these peculiar elements is better known and has
been related to teleostean taxonomy, there remains the possibility that
some of them are derivatives of holostean double cones (Fig. 24a) which
have never quite equalized their two members, rather than a secondary
departure of twin cones in the direction of double ones.

Like the double cones of other classes, the twin cones of the teleosts
appear to be related to diurnal activity. Wunder has shown that they
are most numerous in surface fishes, less and less common in fishes
which habitually swim at greater and greater depths. Thus they seem
somehow to be associated with vision in bright light, though apparently
not with sharp vision since they are excluded from teleost foveae. More
than that cannot be said about them in the light of present knowledge.

Ophidian Double Cones — The double cones of snakes are quite
unique. Though all lizards have double elements of the standard type
(Fig. 25a), the primitive snakes of the boa family have only single cones
of one kind, together with rods (Fig. 69b, p. 167). In the big central
family of snakes, the Colubridae, the standard retina contains only cones
of three types. One of these (Type A) is a large single cone and is
abundant. Another (Type C) is a small single cone which occurs always
in small numbers and is entirely lacking in the retinae whose resolving
power is highest.

The Type B, double, cone (Fig. 24d) bears no resemblance to double
cones outside the snakes. Its chief member is bulky, and is identical
with the Type A single cone. The accessory is extremely slender and is
fused with the chief cone throughout the length of the inner segment.
The accessory nucleus is often displaced laterally in the outer nuclear
layer; and applied to it is an organelle, the paranuclear body, which
occurs only in ophidian double visual cells. Snake cones have no oil-
droplets or paraboloids, and the ellipsoid usually fails to stain with acid
fuchsin. The inversion of size-relationship of chief and accessory, the
paranuclear body, the absence of a paraboloid, and the extensive fusion
of the inner segments set the ophidian double cone off so sharply from all
others that even if it were present in the Boidae one could feel certain that
it was originated de novo within the snake group, and represents the
second — at least — separate invention of a double cone by vertebrates.

62

THE VERTEBRATE RETINA

Double Rods — Still another kind of visual cell is the double rod. These
were long known in geckoes (a family of nocturnal lizards) and have
recently been found in snakes. The gecko double rod (Fig. 25) was

Fig. 25^Double rods in lizards, and their derivation, x 1000.

a, the two cell-types of the pure-cone retina of the (diurnal) collared lizard, Crotaphytus
collaris; parts as in Figs. 22 and 24. The outer segments are tiny and the oil-droplet is
yellow in life.

b, cell-types of Rivers' night lizard, Xantusia riversiana. The outer segments have become
rod-like but contain no rhodopsin, and the oil-droplets are large and colorless. Morpholog-
ically, these elements are intermediate between cones and rods; physiologically, they are
low-threshold.

c, the cell-types (single and double rods) of the banded gecko, Coleonyx variegatus. The
massive outer segments contain rhodopsin, and the oil-droplets have disappeared.

certainly not derived from a bifurcated single rod, but directly from a
double cone. It is thus closely homologous with the ordinary type
of double cone since it is the latter which occurs in diurnal lizards. The
double rods in certain snakes (Fig. 26) were just as certainly derived
from the peculiar ophidian type of double cone, for they have exactly

DOUBLE RODS

the same structure except for the size and shape of the outer segments.
They contain no rhodopsin, and owe their sensitivity to the large vol-
ume of their outer segments and to their multiple connections to single
nerve cells. The gecko double rod does contain a rhodopsin, indicating
that this substance, like other pigments such as hemoglobin and melanin,
can be evolved repeatedly and was not invented once and for all.

This whole matter of the conversion of one type of visual cell into
another will be discussed at some length later (Chapter 7, section D).
It has a considerable bearing upon the ability of animal species to change
their characteristic behavior with respect to light, and upon the question
of the capacity of animals for discriminating colors (see Chapter 12).

Fig. 26 — Double rods in snakes, and their ancestry.

a, the three cell-types of the pure-cone retina of a diurnal colubrid, the European gcass
snake, Matrix natrix; parts as in Figs. 22b and 24d. Type A is the ordinary single cone;
type B is the double cone, equal in numbers to A; type C is an uncommon single cone with
dark-staining ellipsoid.

b, the homologous rod types of the spotted night snake, Hypsiglena o. ochrorhynchus. In
this genus and in some other colubrids, the ancestral cones have all been converted into rods,
through intermediate conditions shown by such forms as Cemophora, Arizona, Rhinocheilus,
and Trimorphodon. See Figure 68a, p. 166.

Since cones can and do change into rods in evolution — and rods into
cones, as well, though less often — it is not surprising that numerous
halfway stages in such derivations occur in living forms. These are, of
course, grist to the mill of those few who insist that any distinction be-
tween rods and cones is wholly artificial. Naturally, such cells do defy
classification, and will not be considered here as discrete types.

64 THE VERTEBRATE RETINA

(C) The Duplicity Theory

History — In 1866 the great retinologist Max Schultze unobtrusively
announced a conclusion to which he had come after some fifteen years
of investigations in comparative ocular histology. He had been struck
by the correlation between the relative numbers of rods and cones in
various retinae and the habits of their possessors with regard to light.
Nocturnal vertebrates had many rods, and few cones or even none.
Diurnal species had ipany cones, and might even lack rods entirely.
Schultze suggested that the cone is the receptor for photopic (bright-
light) vision and that the rod is the organ of scotopic (dim-light) vision.
To this he added a corollary hypothesis that the cone alone is respon-
sible for color vision; for in dim light colors are no longer discriminable
and the world presents itself only in shades of gray.

This theory passed unnoticed by the physiologists and early psychol-
ogists until, toward the end of the century, the same idea was brought
forward independently by two men who were led to conceive it by differ-
ent lines of evidence, and neither of whom knew much of Schultze's
work. Parinaud, studying human vision in certain pathological condi-
tions, produced his 'theorie des deux retines'. Von Kries, repeating and
extending Schultze's observations on twilight vision, with special refer-
ence to the vision of the retinal center, formulated the 'Duplizitats-
theorie' about as we have it at present.

It is not at all uncommon for psychologists and medical men to say
even today that the Duphcity Theory is ^^only a theory," and to express
considerable doubt as to its vahdity. This ordinarily implies a con-
finement of knowledge to the basis of the theory in human vision. Of
course, if one considers only the known facts of human vision, one can-
not expect to be able legitimately to use very many of them to prove the
very theory which was evolved to explain them. But the comparative-
ophthalmological findings of Schultze and of many zoologists since his
time have built so unshakable a foundation for the theory that its major
tenets may be regarded as proven facts. True, there are prominent
French retinologists who do not believe in it, but their methods of study
are so antiquated that it is hardly surprising that they are unsure of the
distinctness of rods and cones.

It is necessary however to bear in mind that the Duplicity Theory as
we state it nowadays is really two theories in one. It states that the rods
are responsible for the hazy, crude, achromatic (black-gray-white) per-

THE DUPLICITY THEORY 65

cepts of dim light and that the cones yield the sharp, detailed images
and the chromatic (colored) sensations characteristic of bright-light
vision. Actually, the factors which make rod vision unsharp but sensi-
tive, and make cone vision sharp but requiring higher intensities of
illumination, are not the same as those which make rod vision achro-
matic and cone vision chromatic. We may be quite sure that animals with
rod-rich or pure-rod retinae have only diffuse mental pictures and can
see in very weak light, but we have at present no proof that all cones
are hue-discriminatory and that all rods are not. To date, no animal
positively known to have only rods in its retina has been properly tested
for color-vision capacity, and many animals which have plenty of cones
have been shown not to have color vision (see Chapter 12, section A).

Sensitivity versus Acuity — When we say that an animal sees well or
sees poorly, that it can see in the dark or that it is blind in the daytime,
we are loosely jumbling together two aspects of vision which should be
carefully distinguished and thoroughly understood. They are indeed so
very different that they are practically mutually exclusive. These two
aspects are visual sensitivity and visual acuity. By the sensitivity of an
eye we mean its ability to respond to weak stimuli, the capacity it has for
continuing to respond to light as that light is slowly dimmed. By acuity
we mean the ability to continue to see separately and unblurred the
details of the visual object as those details are made smaller and closer
together. Sensitivity involves what the psychologist and physiologist call
'threshold of stimulation'; acuity involves what the physicist and opti-
cian call 'resolving power'.

Both the sensitivity and the acuity of the vision of any vertebrate
depend upon the structure and mode of operation of its entire visual
apparatus, including the gross plan of the eyeball, the characteristics of
the dioptric media, the retina, the cerebral structures involved in vision,
and the mental capacity of the animal. But the structure of the retina
sets ultimate, maximal limits upon both sensitivity and acuity which can-
not be exceeded by any sort of manipulation of other parts of the whole
system. We can therefore understand these two aspects of vision well
enough for the time being, if we examine the retinal basis for each.

Retinal Factors in Acuity—To consider acuity first: if the reader
will carefully compare a newspaper picture with one printed on the
glazed paper of a magazine, he will see that each is composed of dots,
and that the two pictures differ greatly in amount of detail. The news-

66 THE VERTEBRATE RETINA

paper picture is built up of large dots spaced widely, for on such rough
paper any finer dots would make only an inky blur. The magazine
photograph contains many more dots per unit area, and they are much
smaller. We say that the magazine picture is the better resolved of the
two. Similarly, we might take two photographs with the same camera
but using two different kinds of film whose emulsions differed greatly
in fineness of grain. The fine-grained picture could be enlarged much
more than the coarse-grained one without becoming blurry and losing
in detail. The fine-grained emulsion 'resolves' better what it 'sees'.
Again, through a well-corrected microscope lens one can see and count
fine dots, striations and the like which run together under less perfect
lenses — and again, we speak of a difference in resolving power as exist-
ing between the two. As we have seen, retinal images are very small;
but mental images are 'big as life' and the retinal image must stand
enormous enlargement without too much loss of detail, when it is trans-
lated into a mental picture of the visual field of the eye.

The dioptric apparatus of the eye may cast upon the retina an image
which is relatively large or small, hazy or sharp; but the retina in turn
may be crudely or finely built and upon this will depend the possible
maximum perfection of the cerebral image. The resolving power of the
retina is governed by three factors, all of which vary from retina to
retina and the last of which may even vary physiologically from time
to time within a single retina: (a) the slenderness of the visual cells;
ib) their closeness of spacing; and (c) the number connected with one
optic nerve fiber. The first two of these are almost self-evident; for if
the images of two object-points fall upon two separate visual cells, be-
tween which is an unstimulated visual cell, the two object-points may
be resolved; but if the visual cells are so plump or so far apart that the
two object-points are imaged upon two adjacent visual cells, they cannot
be distinguished as two points and will seem the same as a single large
object-point whose image covers the same two adjacent visual cells. In
the one case, we have an analogy for the fine screen through which a
picture is photographed for reproduction on coated paper as a half-tone
electrotype; in the other case, a coarse screen like that used with news-
print.

Factor "c" brings in the concept of summation presented in a pre-
ceding Section. Two object-points, whatever their size or separation, will
be seen as a single blur if their images fall upon visual cells which
connect with the same bipolar, or upon those whose separate bipolars

SENSITIVITY VS. ACUITY 67

connect with the same ganglion cell. Other things being equal, the more
bipolar and ganglion cells in a retina, the higher its resolving power.
Two retinae may be about equal in this regard even when one has many
slender, tightly packed visual cells and the other has fewer, plumper,
more widely spaced ones; for in the first retina there might be many
bipolars but few ganglion cells, or fewer bipolars and more ganglion
cells, and the overall resolving power be no greater than that of the
second retina whose visual cells were scanty and large — provided they
had isolated bipolar and ganglion-cell connections.

When sections of the retina are especially prepared so that its nerve
fibers and their connections are brought out, the retinal foundation for
the visual-acuity tenet of the Duplicity Theory is at once evident. Rods
are always connected in large numbers to single bipolar cells while cones
tend to have more isolated connections (Fig. 19, p. 43). Of the many
forms of bipolars in the human retina, the smallest (midget bipolars of
Polyak) each tend to be connected with a single cone and in turn to an
individual ganglion cell and optic nerve fiber, so that each such cone
has a 'private wire' to the brain; whereas, to extend the telephone anal-
ogy, other cones and especially rods are on the old-fashioned multiple
'party line'.

This great difference in the degree of summation of rods and cones
is the most important single factor in making rod vision diffuse and
cone vision sharp. It is much more than enough to compensate for the
fact that in almost all retinae the rods are more slender than the cones,
which would give the rod-population the higher resolving power if the
degrees of rod- and cone-summation were made equal. Thus the chief
reason for the crude character of rod vision is outside of the rod itself;
and we should so state the Duplicity Theory that it attributes acuity
differences not to the rods and cones themselves but to the entire rod-
vision and cone-vision mechanisms, each including a set of visual cells
and their particular bipolars, ganglion cells, and optic nerve fibers.
Relatively few bipolars connect with both rods and cones and probably
a minority of ganglion cells embrace both rod- and cone-bipolars. Parin-
aud's 'theorie des deux retines' is thus really more expressive of the
facts than is 'Duplicity Theory'. The most recent and accurate esti-
mates of the number of rods and cones in one human retina are : rods,
110,000,000 to 125,000,000; cones, 6,300,000 to 6,800,000 (Osterberg).
There are about 1,000,000 fibers in the human optic nerve, not all of
which are sensory; and in a sizable group of these (the macular bundle)

68 THE VERTEBRATE RETINA

each fiber represents a single, unsummated cone. Obviously, summation
is very great even in the human retina — and the human eye is built,
better than most, for 'sharp' vision!

Another important cause of the haziness of rod vision is the dilatation
of the pupil. To have only the rods in action, the illumination must be
dim — below the threshold of stimulation of the relatively insensitive
cones. The pupil opens to let in more light, which permits the rods to
continue in action but, incidentally, has two unfortunate effects: the
'depth of focus' of the eye is reduced, and the periphery of the lens
comes into play with its detrimental effect upon the quality of the
optical image. There is nothing the retina can do about it, and twi-
light vision here suffers another loss in resolution for which the in-
dividual rods should not be blamed. In animals whose eyes are built for
moonlight, this factor may be negligible or absent since the lens is then
large, and the whole area of its surface exposed by the widened pupil
is probably optically 'good'; but the retinal summation factor is still pres-
ent in such animals, and indeed in far greater degree than in ourselves.

Retinal Factors in Sensitivity — The differences between rod- and
cone-vision with regard to sensitivity are, like the acuity-differences,
caused by three factors. They are not unrelated to the acuity-differences,
and in the case of sensitivity two of the factors reside in the visual cells
themselves and only one is extrinsic. The sensitivity-promoting factors in
the rod mechanism are: (a) the size of the outer segment; (b) the
extent of summation; and (c) rhodopsin.

The business end of a rod or cone is its outer segment. It is in this
part of the cell, nearest the pigment epithelium and thus farthest from
the source of light, that the light effects chemical changes which initiate
the impulse that travels down the length of the cell and, if it is strong
enough, evokes a nerve-impulse in the associated bipolar. By and large,
rod outer segments tend to be long cylinders whereas cone outer seg-
ments are shorter (Figs. 22-26) ; and while these may be as thick through
at their bases as rod outer segments, they taper more or less and may
even be quite pointed at their tips. Hence the names originally applied
to the two types of cells, though the human cone outer segment is now
known not to be at all conical when properlv preserved.

If a geometrical cone and a cylinder have the same area of base and
the same height, the cone then has only one-third of the volume of the
cylinder. Here is an important intrinsic reason why, other things being

SENSITIVITY VS. ACUITY 69

equal, a rod should be more sensitive to light than a cone — several times
as much photosensitive material is traversed by a pencil of light, when
it stimulates a rod, as when it stimulates a cone. Thus in dim light
sufficient chemical change may take place in a rod for an effective im-
pulse to reach the bipolar; but the same amount of light will not lead to
activity in a cone-bipolar alongside. The rod, then, will have the lower
threshold of stimulation — it will take less light to set off its transmission
of an impulse. Rods can lower their thresholds in evolution (thus in-
creasing their sensitivity) by lengthening their outer segments as long
as this does not interfere with the nutrition of the rest of the retina from
the choriocapillaris. Cones could of course also increase their sensitivity
by elongating and by approaching a cylindrical form; but they have not
often done so, except as a part of the process of transmuting into rods.

The second factor influencing sensitivity is the extent of summation.
If several visual cells are hammering at the door of a single bipolar, it
is more likely to be aroused than if a single visual cell has to try to evoke
a bipolar response without aid from others. Nerve cells carry impulses
in obedience to the 'all-or-none law', which means that if a given fiber
conducts an impulse at all, it transmits it at full strength. The visual
cells, however, are not nerve cells (see Chapter 5, section B) and there
is no evidence that their foot-pieces obey the all-or-none law. We are
consequently free to suppose that when even a little light strikes a
rod, something happens photochemically, and that several feeble im-
pulses travelling down several rod foot-pieces and impinging upon one
bipolar dendrite can start an impulse flowing in that bipolar. In the same
weak illumination, a single cone or even a rod would not carry an im-
pulse strong enough to awaken a private bipolar.

Indeed, unless the function of the multiple connections of rods to
bipolars is to promote the sensitivity of the whole rod-mechanism in this
way, the inward convergence of the retina becomes quite meaningless.
Summation tends to destroy visual acuity, and no animal needs or wants
diffuse vision for its own sake — he only tolerates it if he must do so in
order to gain the sensitivity which happens to be more important to him.

Bulky visual cells and extensive summation promote sensitivity, but
it is inevitably at the expense of visual acuity. Sensitivity and resolving
power are thus on the two ends of a see-saw, and whatever sends one up,
sends the other down. This relationship holds as well for extra-retinal
structures as for the retina itself; for the big lenses and wide pupils of
some vertebrates, which produce small bright images and lower the

70

THE VERTEBRATE RETINA

overall ocular threshold, reduce acuity; and in others the flat lens which
produces a broad image, spreading over enormous numbers of visual
cells, thereby increases the resolution but at the same time lowers the
brightness of the image and thus reduces the sensitivity of the eye as
a whole.

By far the most important factor in endowing the rods with their
great sensitivity is the substance which is called Visual purple' or better,
rhodopsin. This is a deep red pigment which is formed slowly but con-
tinuously in the rod outer segment. The greater its concentration there,
the more light is absorbed and the more effective is that light as a stim-
ulus for vision. Since rhodopsin is destroyed by light, it builds up to
higher concentration in dim light or darkness than in bright light. Thus

rods alone

(log) Intensity (log) Intensity

Fig. 27 — Evidence for the Duplicity Theory (see text).

the sensitivity of the rods automatically increases just when it will do
the most good, due to the excess of rhodopsin-formation over destruc-
tion, and decreases when that in turn is desirable, due to the excess of
rhodopsin-destruction over formation, in bright light. Moreover, the em-
ployment of rhodopsin for increasing sensitivity does not entail any
sacrifice of resolving power by the rod-mechanism, and there are few
vertebrates whose rods get along without it.

It is rhodopsin which is largely, perhaps entirely responsible for 'dark
adaptation', the familiar result of which is our ability to see quite well
around us in a theater after a few minutes in our seat, although we may
have had to feel to see whether the seat was empty, when we first came in.

Rhodopsin is entirely absent from cones at all times; and there is per-
haps so little of it in rods when they are brightly illuminated that they
must then fall back upon the intrinsic outer-segment-volume factor and

EVIDENCE FOR DUPLICITY OF VISION 71

the extrinsic summation-difference to retain any lead over the cones in
the matter of sensitivity. But when the rods are working to best advan-
tage, at intensities below the cone threshold, the intrinsic factor of their
rhodopsin content far outweighs the combined effect of the other two.
So important is rhodopsin in this regard, and so deeply involved in the
fundamental chemical events of the visual process itself, that a large part
of the first section of the next chapter will be devoted to this magic
chemical whose effect is: "Now you don't see anything; now you do!"

Evidence for Duplicity of Vision — Essentially, then, the Duplicity
Theory states that the retina contains a sensitivity mechanism and an
acuity mechanism, and identifies these with the rods and cones respec-
tively. If both of these mechanisms are in operation only through a

(log) Intensity Time In Darkness

Fig. 28 — ^Further evidence for the Duplicity Theory (see text).

certain transitional range of intensities, and only one or the other of
them can operate effectively below and above this range, we might ex-
pect that many phases of visual physiology would exhibit differences in
accordance with whether one, both, or the other mechanism were
in action. This is indeed the case. When graphs of various visual physi-
ological processes are plotted, a characteristic 'kink' is always to be seen
in the curve, marking the change-over from predominantly rod- to pre-
dominantly cone-control of the process in question. Moreover, when
such curves are plotted for stimuli restricted to the pure-cone (foveal)
portion of the human retina, or are plotted for animals with cone-sim-
plex retinas, there is no kink— the whole curve resembles the cone portion
of the graph of a rod-and-cone, duplex, retina. And of course pure-rod
retinae yield curves which lack kinks and simulate the below-the-kink
portion, or rod portion, of a duplex retina's graph.

72 THE VERTEBRATE RETINA

The kink is often sharper than we might expect it to be, if it repre-
sents a transition. It is accentuated — that is, the overlap of rod-func-
tioning into the physiological realm of the cones is reduced — by little-
understood phenomena of mutual inhibition of rods and cones. Circum-
stances which favor one of the mechanisms allow it somehow to sup-
press, partially, the activity of the other mechanism. Thus the rods or
cones of a 'pure' retina in some ways exceed in performance their
counterparts in a duplex retina.

When the rate of flashing of an intermittent light is speeded up, a
point is reached at which the successive impressions fuse and the light
appears to burn steadily. This 'critical frequency of fusion for flicker'
has been much studied in man and animals — in the latter by indirect
methods, of course, involving training or the recording of the electrical
discharges from the retina. The critical frequency increases with inten-
sity (strictly, with the logarithm of intensity — = Ferry-Porter law) . At
an intensity of 0.25lux— the cone threshold — the critical-frequency
curve of a duplex retina such as the human shows a kink (Fig. 27).
When colored lights are used, the effect of color on the critical frequency
begins to manifest itself only above the cone threshold, as would be
expected. With red light, there is no kink— the rods being insensitive to
deep red, however intense. Only the cone part of the flicker-fusion curve
is obtained from foveal stimulation; and, the farther peripherally the
area stimulated, the closer the whole curve simulates that part due to
the rods alone. A pure-cone retina, such as that of a turtle, gives a kink-
less curve. The pure-rod gecko has also been found to give a homogen-
eous curve — though the curve is that characteristic of cones, which
seems surprising until one takes into account the fact that the geckoes'
rods were secondarily derived from cones (see Fig. 25) .

Another visual phenomenon which plots a kinked curve is the thresh-
old of intensity discrimination. By this is meant the proportion by which
a light must be increased in intensity in order for it to be seen to have
brightened. The initial intensity being designated "I", the increment is
"dl". The curve of "I/dl" plotted against "I" (Fig. 27) shows a change
of slope, or kink, at the cone-threshold intensity. With only foveal
stimulation there is again no kink; nor is the rod part of the curve, or
any kink, obtained with red light.

Perfectly familiar to all is the increase of visual acuity with intensity
— so very commonly do we speak of a light as being "not bright enough
to read by." Less apparent is the existence of a kink in this relationship

EVIDENCE FOR DUPLICITY OF VISION 73

as well, with acuity rising more rapidly above the cone threshold than
below it in most animals (Fig. 28). If we knew very accurately this
relationship for pure-rod and pure-cone animals, we would expect to
find their curves of acuity-versus-intensity to be kinkless.

As a final illustration of the difference in behavior of rods and cones,
we shall consider the rate of dark adaptation, or increase in sensitivity
in darkness following exposure to bright light. The graph of this in-
crease (Fig. 28) again shows a fairly well-defined kink owing to the fact
that the cones reach their maximum sensitivity at a rapid rate before the
sensitivity of the rods begins, slowly, to increase at all. In pure-rod,
duplex, and pure-cone eyes the expected differences in the slope of the
curve, and in the presence or absence of a kink, are indeed found when
such criteria of sensitivity as the behavior of the pupil or the electrical
discharges from the retina are recorded.

We have surely seen enough evidence now to convince ourselves
of the duplicity of the visual process. The complexities of the above
evidence may seem rather appalling to the innocent reader; so, let us
try, in the next chapter, to make the process of vision seem fairly
simple after all!

Chapter 4

THE VISUAL PROCESS

(A) ScoTOPic Vision

Any attempt to depict the events which intervene between the impact
of Ught upon the retina and the registration, in consciousness, of the
quahtative and quantitative aspects of vision, must necessarily be largely
guess-work, and can be lucid and connected only if it is dogmatic. The
following treatment is such an attempt, made for the sake of the reader
rather than for the sake of the subject. The literature of the field of
visual physiology is vast and unorganized, and largely unreadable with-
out a considerable background of mathematics. Paraphrased sans mathe-
matics, it is bound to seem largely a series of unfounded generalizations
to any astute physiologist who may read it; but, these latter gentry have
yet to promulgate an inclusive theory of vision in which a sophomore
cannot pick great holes. In the present state of knowledge, one descrip-
tion of what goes on in vision is almost as good as another, and may be
the best one for the beginning reader if, at least, he is able to follow it
without miring down in equations.

Rhodopsin — Perhaps the greatest advance which has ever been made
in this field was the discovery of the photosensitivity of the rod pigment,
rhodopsin, by Boll in 1876, and the elucidation of most of its properties
by Kiihne in the years immediately following. But rhodopsin was at first
used to explain too much, and during its history many of its original
attributes have had to be taken away from it. Physiologists have relin-
quished their beliefs about rhodopsin most reluctantly, since the less one
can credit to it, the farther away seem the solutions of some of the
fundamental problems of vision. However, in very recent years some
progress has been made in the study of other photosensitive substances
in the retina, which may be found to do some of the things formerly
credited to rhodopsin itself.

Rhodopsin was once supposed to be the sine qua non of all of verte-
brate photoreception, and owing to the attention it commanded, photo-
chemical theories of vision rapidly came to be the only ones seriously
considered. But it was soon seen that if vision does have a strictly photo-

RHODOPSIN 75

chemical basis, no one photosensitive substance could be entirely respon-
sible for color vision — at least three such substances are required by the
long-popular Young-Helmholtz theory, and even more were demanded
by some other theories of color vision. Rhodopsin might be one of these
— but where were the others? The resuscitation of Schultze's ideas in
the form of the Duplicity Theory made it necessary to abandon rho-
dopsin as a color-vision photochemical, for it was finally made certain
that some vertebrates have none of it, and that it never occurs in cones.
Still, there were those who believed that vision as such — brightness-
vision both photopically and scotopically, apart from hue perception —
necessitated rhodopsin. These workers argued that there must be in-
visible traces of the substance in cones in order to account for their
light-sense; and this idea has been very long a-dying.

Rhodopsin is still widely regarded as the absolutely essential photo-
chemical substance for rod activity. Even this is an unnecessary belief,
since rhodopsin may be nothing more than a sensitizer, so powerful that
its action masks that of another, essential, material so completely that the
brightnesses of lights are directly related to their effects upon rhodopsin.

The substance is a reddish pigment whose chemical nature is not yet
completely known. It is released from the rod outer segment by sub-
stances which lower surface tension, such as bile salts, saponin, digitonin,
sodium oleate and salicylate, and snake venom. It forms a precipitate
with platinic chloride — an insoluble yellow compound which can be seen
in the rods in permanent microscopic preparations made of retinse which
are kept in darkness for an hour or so before preservation.

Rhodopsin is commonly described nowadays as a hydrocarbon con-
jugated with a protein, through a belief that vitamin A — essentially a
hydrocarbon — is an important constituent (r. /'.). The molecular weight
of rhodopsin is about 270,000. This and other features make it clear
that most of the molecule is proteinous; but of course to say that rho-
dopsin is essentially a protein is like saying that dynamite is essentially
fuller's earth. The business part of the molecule — its 'chromophoric'
(color-bearing) group — is neither a hydrocarbon nor a protein, though
it may be derived indirectly from a portion of the vitamin A molecule.
The latest information* is that the rhodopsin molecule contains a pro-
tein, 'provisual red', and probably a third substance. The chromophore,
provisual red, can be split into a fatty acid and 'visual red'; the latter in

'''Kindly supplied b>- Dr. Arlington C. Krause in advance of his own publication thereof.

76 THE VISUAL PROCESS

turn can be made to yield Visual yellow' and 'indicator yellow'. Certain
of these photosensitive substances have previously been identified as
partial-breakdown products of rhodopsin when it is struck by light.

The most important properties of rhodopsin are its intense colored-
ness, its sensitivity to all visible wavelengths excepting those deep red
ones which (by reflection from it) give it its own color, and the fact
that its response to these wavelengths is to disrupt into colorless or pallid
substances of little or no photosensitivity. It is most affected by the blue-
green region of the spectrum, centering at about A500m|l. One might
expect that this wavelength would appear brightest to the dark-adapted
eye in which rhodopsin has built up to a high concentration. Owing how-
ever to modifying factors (chief of which is believed to be the high
absorption of short-wave light in the ocular media), the brightest point
in the scotopic spectrum is shifted red- ward, to ?L510m[i. One of the two
or more substances into which rhodopsin is broken down by light is
presumed to irritate the protoplasm of the rod and cause a wave of
electrochemical activity, much like the impulses which flow along nerve
fibers, to pass down the rod foot-piece and stimulate the bipolar neuron.

Dark Adaptation — Rhodopsin is not as all-important as it was once
thought to be, but it is largely responsible for the ability of the rod to
'dark-adapt' or lower its threshold — until the amount of light needed to
stimulate it is a tiny part of that required to arouse a cone. While we are
in ordinary daylight there is believed to be but little rhodopsin in our
rods, for the concurrent processes of its synthesis and breakdown are
then in equilibrium at a sub-maximal concentration of the substance.
When we enter a dark place the process of adaptation to dim light
begins at once, since the breakdown all but ceases while the upbuilding
of new rhodopsin continues at the usual rate. In the dim light, a new
balance is struck at a high concentration of rhodopsin, so that a given
amount of additional light will now appear brighter than before, since it
destroys a greater absolute amount of the photosensitive pigment.

Rhodopsin is not quite the whole story in dark-adaptation, however.
The dilation of the pupil, upon going into a dim or dark place, admits
more light to the retina, so that the overall sensitivity of the eye in-
creases somewhat, apart from any change in the retina itself. In the latter,
the first step in dark adaptation is taken by the cones rather than the
rods, for the tiny amount of photosensitive material which they ever
contain is very quickly built up to a maximum (see right half of Fig. 28) .

DARK ADAPTATION 77

Then, too, a part of dark-adaptation — it is hard to say how much — is
accompUshed by switchboard effects in the integrative layers of the
retina, bringing about temporary hook-ups, to gangUon cells, of larger
numbers of visual cells than usual.

In dim light or darkness, the destruction of rhodopsin having largely
or wholly ceased, the new formation of the substance (partly from the
decomposition products still present in the rods, partly from new raw
material absorbed from the pigment epithelium) quickly restores the
concentration to a fairly high level. Within seven or eight minutes, in
fact, the previously depleted rod becomes capable of function. The rods
are now deeply colored and absorb much more of whatever light may
strike them, so that a strong impulse impinges upon the bipolar. Should
we now emerge into a bright place, the light would dazzle us uncomfort-
ably until enough rhodopsin had been destroyed to raise the thresholds
of the rods considerably. This process takes a much larger fraction of
a second than is required for the pupil to constrict. So, the removal of
some of the rhodopsin is the controlling factor in /zg/?/-adaptation —
which we might loosely define as the destruction of excessive sensitivity.
The pupil slowly reopens as the sensitivity of the retina is decreased, and
attains a final 'physiological size' appropriate to the particular species of
animal, and which for man is maintained in all intensities between 100
and lOOOlux — the range within which, presumably, an equilibrium can
be maintained in the photochemical system of the visual cells.

Rhodopsin accumulates to a considerable proportion of its maximum
in half an hour and is almost at maximum in an hour; but it continues
to form slowly for twenty-four hours or more. If anything essential for
its manufacture is deficient in the individual or in his diet, the rate of
formation will be greatly retarded, and the greatest amount ever formed
will be much less than normal. This condition of deficiency leads to
nyctalopia or night-blindness, in which dark-adaptation is incomplete
and the individual feels the handicap when trying to make his way about
in dim places and at night. He may become a menace to his fellows if
he drives an automobile at night and meets many bright headlights
which assault the little rhodopsin he is able to form. In the armies of
years ago, night-blindness — common under conditions of malnutrition —
automatically exempted a soldier from nocturnal guard duty. In modern
warfare, the night-blind individual is particularly useless in defense
against nocturnal bombing, and every effort is made to maintain a high
concentration of rhodopsin in the retinae of night fighter aircraftsmen.

78 THE VISUAL PROCESS

The substance whose lack is the usual cause of nyctalopia was shown
in 1925 to be vitamin A, a colorless material manufactured in the liver
from carotene, a reddish plant pigment. Although there are types of
nyctalopia which are hereditary, and the condition also occurs as a symp-
tom of degenerative retinal diseases, in its various degrees it is usually
the first detectible sign of vitamin A deficiency. Nutritionists and pedia-
tricians are consequently much interested in attempts to devise clinical
tests— by which they mean quick and easy ones — for nyctalopia; but
for various reasons a reliable test which is really simple seems hardly
possible, and the literature of the subject reveals more and more pessi-
mistic statements.

Soon after 1925, the obvious conclusion was drawn that vitamin A
is the precursor of rhodopsin, that it is actually converted into that
substance, and may be formed again when rhodopsin is disrupted by
light. Elaborate diagrams of this closed circuit, with the supposed
intermediate compounds, are commonly seen in print. But the most
recent and careful chemical studies of rhodopsin itself (r. s) have great-
ly weakened our faith in a direct genetic relationship between it and
vitamin A. All that can be safely said at the moment is that the vitamin
is essential for the synthesis of rhodopsin, probably as a minor contrib-
utor rather than as a principal raw material.

Rhodopsin may be the essential, the one and only photochemical sub-
stance that is ever present in rods, but there is no proof that this is
so. There are rods which contain none, though perhaps in all of these
{e.g., in Sphenodon, Xantusia, Phyllorhynchus) the lack of rhodopsin
is owing to these rods' having had relatively recent origin from cones.
They presumably get along perfectly well with the photochemical system
inherited from their cone ancestors — for all anyone knows at present,
the complete color-vision mechanism may still be functioning in them.
The photochemical substance or substances in cones may indeed have
chemical kinship with rhodopsin, for it has recently been reported that
the dark-adaptibility of the cones (which in terms of intensity-limit ratios
is actually about equal to that of the rods) is influenced by the dietary
intake of vitamin A.

Just a few years ago, it was being claimed by the Finnish retinal
physiologists associated with Ragnar Granit that when a rat retina has
been so brightly illuminated that all of the rhodopsin is bleached, the
optic nerve no longer carries the electrical discharges which can normallv
be detected in it during photic stimulation of the retina. This was hailed

ROD VISION 79

as proving conclusively the complete dependence of rod vision upon rho-
dopsin. But workers in the same laboratory have more lately obtained
puzzling indications that very little rhodopsin is ever normally bleached
in the intact animal. They found apparently normal amounts of it in
eyes whose electrical responses had been reduced one-third to one-half
by stimulation with light. Possibly the electrical responses would entirely
disappear while there was still a great deal of rhodopsin in the rods.
This might be new evidence that rhodopsin is a secondary sensitizer
rather than a primary photosensitive material, or it might only mean
that switchboard effects in the retina are more important in light-adapta-
tion than we have been supposing.

Whatever its whole meaning may be, rhodopsin was a clever invention;
for its light-absorbing power makes it responsive to weak light, yet it
conveniently bleaches when, in bright light, the full amount of it would
greatly handicap the animal. Even the particular color it possesses is in
itself adaptive, as will be elucidated later (Chapter 12, section A).
So elaborate a substance could hardly have been present in the 'original'
provertebrate visual cell, which must then have been high-threshold, more
like the cones we know than like a modern rod. Some of the photosensi-
tive ancestor-cells of the rods and cones were left behind in the brain
lining when the eyes evolved, as will be brought out in the next chapter.
These, though sensitive enough to respond to light through the entire
wall of a bird's head (as shown by their reflex control of spermatogenic
activity), contain no rhodopsin as far as we know. If the modern rod
cell depends utterly upon rhodopsin for its photosensitivity as such, it
has come to do so secondarily by discarding some more ancient photo-
chemical for want of efficiency under scotopic conditions.

Rod Vision — We may conceive of the peripheral (ocular) portion of
the rod visual process as taking place somewhat as follows : At the start
of adaptation to dim light there is little rhodopsin in the rods, and so
little of this is broken down by the weak light that only feeble impulses
pass down the foot-pieces. As the amount of rhodopsin increases, a
greater absolute amount is broken down by a given light and the im-
pulses become stronger. Those bipolars with which the largest numbers
of rods connect now receive enough total stimulation to be set off into
conductive activity, and they begin to carry nerve impulses at a certain
low frequency of discharge — each bipolar acting somewhat like a reser-
voir and, so to say, filling up with stimulation and discharging an im-

80 THE VISUAL PROCESS

pulse, the frequency of discharge thus bearing a relation to the amount
of stimulation.

The attached ganglion cells now behave similarly and conduct in
synchrony with the activity in the bipolars. The electrical aspect of their
discharges can be picked up in the optic nerve as action currents
with proper amplifying and recording devices. In the brain, a sensation
of light is now aroused whose strength depends upon the resultant of
the number of active nerve fibers and their frequency of discharge. As
dark-adaptation proceeds further, the number of rods per unit area of
the retina whose activity actually registers in consciousness steadily in-
creases, due to the activation of more and more bipolars having smaller
and smaller numbers of associated rods. As the mosaic of functional
receptor units becomes more and more dense, visual acuity rises hand in
hand with the rise in the strength of the brightness sensation. When
dark-adaptation is complete, both visual acuity and brightness are max-
imal for the intensity being supplied, and any further increase in either
will depend upon an increase of illumination above the threshold of the
cones, thus bringing the latter into play. The destruction of rhodopsin
may then increase to such an extent that the brightness would decrease
in the face of increasing objective intensity — in other words, light adap-
tation would have commenced. Incidentally, rising intensities above the
cone thresholds naturally bring into action more and more cone bipolars
and associated ganglion cells, so that visual acuity continues to rise until
all elements are functioning. Beyond this point, further increase of in-
tensity brings no additional visual acuity — though of course brightness
can increase until all involved optic nerve fibers are discharging into
the central nervous system at their maximum rates.

If, with the retina thoroughly dark-adapted, it is now subjected to
bright light, rhodopsin is immediately broken down in large amounts in
all of the rods which are receiving stimulation, and all of their associated
nerve fibers begin to conduct at high frequency. As the rhodopsin fades,
however, the rod thresholds rise and the frequency falls off. As the rod
thresholds approach those of the cones, a comfortable brightness is
attained with the pupil now reopened, and with the rods perhaps still
all in action, contributing all that they ever can to the resolving power
of the retina — considering that they are of course still summated. In
comfortable illuminations above the cone threshold, however, the cones
are contributing only a part of their potential resolving power, which
becomes maximal only at intensities above 100 lux.

CONE VISION; COLOR 81

(B) Photopic Vision

Cone Vision — Turning now to the cones, we are confronted with the
complex matter of color vision — assuming for the nonce that all cone-
bearing vertebrates do discriminate hues. We can imagine subtracting
color vision from the whole performance of the cone — but what we
would have left, we could describe in terms of a rod mechanism that
had little summation and very little rhodopsin. So, we cannot well avoid
considering the elementary and purely qualitative aspects of color vision
if we are to attempt to picture the mechanism involved and thus round
out our survey of visual physiology.

Color — Color, or better, 'hue', exists only in the mind. No light or
object in nature has hue — rather, the quality of hue aroused as a sen-y
sation is projected back to the object as one of its attributes, just as the
patterns of brightness and darkness in consciousness are projected back
into the visual field to endow objects with their size, shape, tone values,
and movement. For, we perceive objects rather than lights. We can
see objects falsely as to size, shape, and motion, and just as falsely as
to color since color is purely subjective. The color of a surface depends
not only upon its chemico-physical nature, but also upon the kind of
light by which we see it, and upon our memory of the impression it
may have given us under some more familiar illumination. Thus, a par-
ticular dress may look red only in daylight, yet we still call it red under
an artificial light when it may actually be reflecting more yellow light
and should then be seen as orange.

The hue sensation aroused by a light depends primarily upon the
frequency of its vibration, usually expressed as the distance between
successive waves in the vibration, the wavelength. The longest visible
wavelengths, in the neighborhood of 760m|,i, arouse the sensation we call
red; the shortest ones, around 390m[l, give us the sensation of violet,
which must be seen in a spectroscope to be appreciated (since the violets
of textiles and pigments in general are not true violets, but diluted pur-
ples). In-between wavelengths give us the other hues of the spectrum.

When all of the visible wavelengths are being received on the same
area of the retina, either simultaneously or in such rapid succession that
their physiological images persist long enough to overlap or fuse, we see
what we call white light. The removal of some wavelengths from the full
assortment makes the remainder of the light appear, collectively, as a
color. Such a removal may be effected by selective reflection or by selec-

82

THE VISUAL PROCESS

tive transmission. An opaque colored paper or cloth performs the former,
a translucent colored glass or liquid performs both. A colored object is
colored, instead of gray, because it absorbs some wavelengths and reflects
or transmits others. The latter being the ones which reach the eye, they
determine the color of the object. If the object is specially illuminated
only by wavelengths which it can absorb, it can reflect none of them and
will then appear black. An object which in sunlight appears black must,

g yor

Fig. 29 — The physical and psychological spectra.

a, the visible spectrum as formed by a prism.

V- violet; b- blue; g- green; y- yellow; o- orange; r- red.

b, the psychological color circle. Red and violet intergrade through purple; diametrically
opposite hues are complementaries, and make white when mixed in correa amounts.

c, the linear spectrum formed by a lens. The distance from the focus of violet to that of
red (greatly exaggerated in the diagram) is the 'linear chromatic aberration' of the lens.

then, be one which absorbs all wavelengths, just as white objects, to ap-
pear white, must reflect all. Of course no object absorbs or reflects all of
the light striking it. Whether it reflects all wavelengths equally, or some
more^han others, it reflects only a certain percentage of the light energy.
This percentage is the object's reflection coefficient or 'albedo'.

No object can reflect only a single wavelength, and hence no object
Y" can have a pure color. To obtain pure colors, we must select them from a

COLOR 83

band spectrum by means of a slotted diaphragm. Such a spectrum is
formed automatically when a mixture of wavelengths, such as sunlight, is
passed through a narrow slit and then through a prism. Since the refrac-
tive index of the glass is different for each wavelength, being highest for
violet and lowest for red, the colors are sorted out of the mixture and
can be caught on a screen, all in order, as a spectrum (Fig. 29a). If
the light reflected or transmitted by a colored object is concentrated and
passed through a prism, the spectrum formed will naturally have lightless
regions in it corresponding to the wavelengths whose removal from the
sunlight, through absorption by the object, gave the latter its color. Such
a spectrum is an 'absorption spectrum', and is the basis of spectral anal-
ysis, that powerful weapon of chemistry and astronomy with which sub-
stances are detected by means of their specific fingerprints on sunlight.

With a little practise, a normal person can learn to distinguish about
one hundred and sixty distinct hues in the sunlight spectrum.* If we now
let any two of these hues escape through narrow slits and aim them with
mirrors at the same piece of paper or ground glass, or look at one with
each eye, or present them in rapid alternation to one or both eyes, we
will obtain a sensation different from that given by either hue alone.
In most cases, the sensation will be that afforded by some other pure
hue, lying between the chosen two in the spectrum. If however the latter
are far apart in the spectrum, and lie diametrically opposite each other
on the 'color circle' (Fig. 29b), they are 'complementaries' and their
mixture will produce white light. Thus any hue in the spectrum (and
white) can be produced by mixtures, made by one means or other, of some
two other hues. Some white light may need to be added to the spectral
hue in order to make it an exact match for the mixture. We are not of
course discussing here the subtractive mixtures which one obtains by stir-
ring pigments together — the artist's complementary, primary, and second-
ary colors have nothing to do directly with those of the physiologist.

The physiologist often terms red, green, and violet 'primary' colors,
because in none of them can any other hues be seen. Yellow is also con-
sidered a primary by psychologists, as is blue for that matter. Yellow
sensations can be produced by means of simple apparatus which presents
red to one eye and green to the other, but yellow is not reddish green or
greenish red. Yellow, in this instance, is obviously synthesized in the

'''Actually, 160 complexes of hue-plus-whiteness. No one has ever yet determined the (much
smaller) number of hues which would still be discriminable, were saturation eliminated
as a variable.

84 THE VISUAL PROCESS

brain — probably also, as we shall see, even when it is excited monocularly
by monochromatic yellow spectral light. We can, if we like, make an
artificial distinction among the psychological primaries, between those
which can be easily produced by mixtures and those which cannot; but
even red and violet, though at the ends of the spectrum, can be produced
by mixtures. The spectrum really has no ends — it only seems to have,
due to the way in which a prism forms it. Really, it is a closed entity, for
red and violet are adjacent, psychologically — their mixture results in
purple, which lies outside the spectrum but fills the gap between red and
violet in a spectrum which we might imagine bent into a ring (Fig. 29b).

Though the primaries can all be synthesized, they cannot be analyzed
— which is what makes them primaries. In orange one can discern both
the red and yellow components; in purple, the blue and red. But though
blue can be made by mixing green and violet, it does not look as though
it contained either. Yellow and violet, and red and green, are sometimes
called 'disappearing color pairs', since when the members of such a pair
are mixed, neither member can be seen in the mixture.

The mixture of three properly chosen primaries (the most convenient
are red, green, and violet — and these three do have, in a certain way,
an edge on the other two chief primaries, yellow and blue) arouses the
colorless sensation of white or gray, which is also afforded by mixed
complementary pairs of colors such as orange and green-blue, green-
yellow and violet, red and blue-green, etc. In each such pair it can always
be noted that at least one member is not a simple color or primary; and
the two members, between them, always contain red, green, and violet or
can be matched by mixtures of them in pairs. The complement of any
hue can also, obviously, consist of white light minus that hue. A mixture
may be complemented by a pure hue, and the latter by one other pure
hue, by simple or complex mixtures, or by white minus the first pure hue.

Saturation — The whole of the sensation aroused by a colored light or
object has aspects other than hue itself. It has brightness of course, the
psychological counterpart of physical intensity as with achromatic stim-
uli; and it has saturation. Saturation means coloredness as apart from
color, and quite apart from brightness. In a darkroom we could aim,
at the same ground-glass, a beam of pure colored light and a beam of
white light. The ratio of color to white in the resulting spot of light
would be the measure of its saturation. With more white added, the
saturation would go down and the brightness would go up; but instead

SATURATION 85

of simply adding more white light, we could add some white and sub-
tract some colored light, and thus lower the saturation while keeping
the total brightness constant. Again, we could reduce the amount of
colored light without adding extra white, and thus reduce both satura-
tion and brightness. Thus it can be seen that the saturation of a colored
light has nothing to do with the particular hue involved, and is also
quite independent of the brightness.

There are two chief ways in which saturation and unsaturation may
be manifested. Firstly, saturation can represent the extent to which a
spectral color is free from objective adulteration with white light, or the
extent to which a pigmentary color is devoid of admixture with white.
Unsaturation of a colored light-beam by mixture with a white beam has
been mentioned above. A paper- or cloth-color which reflects much light
throughout the spectrum in addition to the strong band of wavelengths
which gives it its hue, is a 'tint' of that hue — unsaturated by the white
it reflects. An artist, mixing Chinese White with an oil color, is un-
saturating that color. Likewise, pigmentary colors may be apparently
unsaturated by mingling them with black, thus yielding 'shades' of their
colors. Admixture with black is really, however, not true unsaturation
but is more nearly tantamount to simply reducing intensity and therefore
brightness — it is like mixing a light-beam with darkness, which would
not unsaturate it even if it could be done! Psychologically, admixture
with black is not quite equivalent to reducing intensity, for blackness
and darkness are not psychologically identical. Brown, for example, is
a black-adulterated color which can be seen as brown only when the
conditions are right for seeing black. In a darkroom, a brown area which
is not surrounded by lighter areas appears simply as weakly orange or
reddish, for the blackness element of the brown becomes mere darkness.
If blackness is 'induced' in an orange area by surrounding the latter with
white in a darkroom, one can obtain the sensation of brown without
resort to pigments, for the orange spot in question need not be pig-
mentary— it can be formed by filtered or spectral light.

It is important, in thinking about saturation, to keep one's attention
upon the amount of color, the 'chroma', present — not upon the character
of the unsaturating factor present, for this does not matter. It need not
even be whiteness which unsaturates, for, if we wish, we may speak of
unsaturating a hue with another hue, and thus think of orange as a red
unsaturated with yellow; but this is more than a little dangerous since

86 THE VISUAL PROCESS

SO many mixed pairs of colors produce sensations which are not analyz-
able blends of their qualities, but entirely new qualities.

Apart from the kind of unsaturation which may be produced syn-
thetically so to speak, by mixing into a color some whiteness from a
separate source entirely outside the color, there is a type of unsaturation
which is inherent in the colored light itself, even in a spectral light of
whatever purity. It is as though the monochromatic spectral beam con-
tained some white light which we could not remove. This kind of un-
saturation is due to the fact that the visual mechanism for the perception
of white is set in operation to some extent by any one wavelength — to a
greater extent by some than by others. If we look at a solar spectrum,
the yellow region (about A,580m[i,) looks brightest to us, and also looks
the least richly colored. We can separate this pallidity of yellow from
its high brightness, by turning to a spectrum in which each wavelength
represents the same amount of energy. In such a spectrum, the yellow-
green region (around A<557m[x) is now the brightest; but the yellow still
seems the least colored color, the richness of the chromas increasing from
it toward both ends of the spectrum.

This kind of unsaturation, or low chroma, is particularly important
physiologically and psychologically. It greatly influences the results of
color-mixtures, for the saturation of mixtures is always low. If for exam-
ple we mix red and green to make yellow, the yellow we obtain is of
low saturation as compared even with spectral yellow, and to spectral
yellow we must add some white light to make a perfect match with the
red-green mixture. The more complex a mixture, the lower the satura-
tion, for we are approaching the result of mixing all wavelengths — which
is, of course, white itself, with the chroma-content at zero.

The degree of saturation of a spectral light can be ascertained by
determining how much of it, added to white, will give that white a hint
of chroma. By such means, red and particularly violet are revealed as
highly-saturated wavelengths, yellow and green as being of low chroma.
We therefore say that the 'white valence' of yellow is high, by which we
mean that we can add yellow to another color without altering the hue
much more than if we had added the same amount of white. Red or
blue, added bit by bit to another color, have more prompt effects upon its
appearance — they have a low white valence, cannot take the place of
very much white in mixtures.

Recalling that unsaturation is usually accomplished by actual objective
admixture with white, we can now see that when the degrees of unsatura-

BRIGHTNESS; THE PURKINJE PHENOMENON

87

tion of two 'pure' hues are compared, we are really comparing their
intrinsic subjective white-sensation-arousing power, their white valences,
or their nearness to whiteness. Yellow is not white, but it is more like
white than red is, because yellow stimuli more effectively stimulate the
whole white-seeing mechanism of the cones and their central connections.

Brightness and the Purkinje Phenomenon — Brightness has the
same meaning in cone-mediated sensations that it has in achromatic rod
sensations, and is just as independent of actual physical intensity. But

THE PURKINJE PHENOMENON
Dark Adaptation Produces

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Fig. 30 — Graphic depiction of the changes which comprise the Purkinje phenomenon.

the relation of brightness to intensity is different for the cone- and rod-
mechanisms. While the brightest part of an equal-energy spectrum is the
yellow-green for the cones, it is in the green for the dark-adapted, func-
tionally pure-rod eye. This shift results in a change in the relative bright-
nesses of colored objects as intensity drops below the cone threshold or
rises above it. This change is the 'Purkinje phenomenon', which is simply
a betrayal of the change-over from predominantly cone vision to rod
vision (Fig. 30; and see Fig, 35, p. 102). It naturally occurs only in
duplex retinae, or duplex retinal areas, and its occurrence is a part of the
great mass of evidence for the Duplicity Theory.

88 THE VISUAL PROCESS

It is only by coincidence that the Purkinje shift has the particular
extent that it has, in any given retina. The luminosity maxima of the
scotopic and photopic spectra might just as well happen to be farther
apart in wavelength, or closer together; or even, by chance, identical,
for they are determined by very different factors. In the one case, the
maximum is determined by the maximum of absorption of rhodopsin —
in the other case, by the peak in the resultant absorption spectrum of
the photochemical substances in the cones. In some animal with a rho-
dopsin of slightly different color, and with a slightly different color-
vision system, the Purkinje shift might be much greater or much less
than in man — or could conceivably be absent (or even might take place
in the opposite direction, though no such case is known.)
f Trichromatic Vision — The fundamental qualities of cone-mediated
sensations, then, are hue, saturation, and brightness. At least a part of
the whole process by which these qualities are established in conscious-
ness is essentially physiological. A part of the process is psychological.
It would be very nice, considering the avowed scope of this book, if we
could carry our treatment of cone vision just to the boundary line and
stop. But unfortunately there is no branch of psycho-physiology in which
it is more difficult to say where more-or-less 'physiological' sensation ends
and strictly 'psychological' perception begins. Some hues, such as red,
green, and violet, appear to be simple sensations. Others, like orange
and yellow-green, are mixtures analogous to the sour-sweetness of lemon-
ade or to a chord in music — trained observers can always discriminate
the separate elements of the complex. But then there are hues, pure
yellow and pure blue, which seem to be more like percepts than sensa-
tions, for each is the product of two simultaneously-evoked sensation
elements, yet cannot be analyzed into those elements. Here, the sum
differs from its parts in a qualitative manner — it is as though when we
hybridized horses with zebras, the offspring were always giraffes!

Since the sensations of all hues and white can be aroused by appro-
priate mixtures of three wavelengths — primaries — chosen from the ends
and middle of the spectrum, normal human vision is said to be trichrom-
atic (tri = three) . It was an eighteenth-century French printer, LeBlond,
who discovered (through a misinterpretation of Newton's writings) that
with only seven colored inks, and black, he could print pictures contain-
ing the whole gamut of colors theretofore obtainable only with a legion
of inks. Being a very economical person, LeBlond experimented further
and found that he could get along with only three colored inks. Thomas

TRICHROMATIC VISION 89

Young formulated a theory of color-vision based upon LeBlond's find-
ings, in which he proposed three sets of receptors in the retina, each
most sensitive to one of three primary colors. Sensations of non-primary
colors were regarded as due to the simultaneous enaction, to varying
extents, of two or all three sets of receptors. Whiteness was due to the
equal stimulation of all three.

Much support for this three-component theory of color vision was
given by Helmholtz in the last century, and nowadays the theory goes
under the hyphenated names of the two men. The Young-Helmholtz
theory calls for three 'somethings' in color vision; but ideas have
changed, from time to time, as to what these somethings are. Young
thought of them as three kinds of nerve endings. Helmholtz thought of
them as three photochemical substances or processes, which he at first
believed to be in three separate sets of cones. Later, he considered that
they probably all occurred in each cone.

Other theorists have complicated matters considerably and, in the
light of the most recent developments, unnecessarily. The perception of
yellow, white, and black formerly gave much trouble and seemed to call
for a minimum of four components in cone vision, as in the theory of
Hering, the principal rival of that of Young and Helmholtz. The binoc-
ular fusibility of red and green into yellow, and the modern concept of
the difference between blackness and darkness as being due wholly to con-
trast, makes the assumption of more than three components unnecessary.

It is entirely likely that the three processes are mediated through each
and every cone. White stimuli do not take on hue when made very small
in area, as we should expect them to do if they then struck only one or
two out of a total of three or more kinds of cones. Again, if there were
three kinds of cones with respect to color sensitivity, visual acuity would
necessarily be very low in a monochromatic illumination which effec-
tively stimulated only one-third of the cones. But visual acuity is not
lower in any monochromatic light (except, perhaps, red) than it is in
white light of equal objective or subjective intensity; and in some such
lights it is even higher. This could mean, as Hecht claims, that all the
cone-types respond nearly equally to any given monochromatic light.
It can also mean that the cones are all alike — at least in any given small
retinal area. They may vary progressively along meridians of the retina,
for the number of hues we can discriminate diminishes from the center
toward the ora terminalis, unless the intensity is very high. Even this
'deficiency' may really have its basis far from the cones themselves.

90 THE VISUAL PROCESS

Binocular color mixture has been mentioned above, in the instance of
the binocular fusion of red and green into yellow. Its existence is fatal
to any theory which places the color-vision mechanism entirely in the
periphery of the visual apparatus — that is, in the retina. There is no
color-sensation, which can be produced by mixing two lights in one eye,
that cannot be duplicated by supplying the two lights, independently,
one to each eye. If color-mixture can be made centrally, one wonders
whether all color-mixtures, even monocular ones, may not always be syn-
thesized centrally. To suppose so necessitates believing that the optic
nerve fibers can simultaneously carry several separate 'primary' kinds
of information, which are integrated into a perceptual whole only after
reaching some level in the central visual apparatus. To account for
binocular color-mixture (and, it can be allowed to account also for
monocular mixture) a multiple synthetic mechanism must exist centrally.
But it would seem difficult for any one photochemical substance in the
cone to be able to give rise to more than one kind of optic nerve impulse.
To account for the transmission of simple primary impulses along the
optic nerve, when the retina is being illuminated by such a mixture as
purple, there must also be a multiple, differentially responsive analytical
mechanism in the periphery.

The binocular synthesis of mixed colors and white results in sensa-
tions identical with those aroused monocularly by the same stimuli. One
reason for this could be that the vision of even one eye by itself is
actually carried out through the binocular (fusion) 'center'. This sounds
roundabout and improbable, but there is considerable evidence for it.
It is difficult to explain otherwise why things look no brighter to us
when seen with two eyes than with only one. The functioning of one eye
can affect the way things are seen with the other eye. To give only one
example: the convergence of a shielded eye causes an apparent lateral
movement of a spot of light seen, in a darkroom, only by the other eye
— especially when the non-seeing eye happens to be the individual's
master or dominant eye. The brain is so accustomed to ascribing most
of vision to the dominant eye, that it can be deceived into supposing
that eye to be seeing even when it is not, and thus 'sees' the spot of light
move in just the way it would have to, to remain visible to the dominant
eye during the latter's rotation. The brain is confused as to which eye
is seeing what, which could only be possible if the two eyes always
formed a team even when only one member of the team works.

TRICHROMATIC VISION 91

The manner in which a mixed color, for instance purple, may be seen
by one eye (or both) presented with purple, or with one eye offered red
and the other violet, is diagrammed in Figure 31. The purple stimulus
in 'a' may of course be steady, or may consist of rapid alternations of
red and violet lights; for, as mentioned earlier, fusion of colors may
occur temporally as well as spatially. When purple strikes a single retina,
impulses somehow tagged 'redness' and 'violetness' pass along the optic
nerve to be combined into 'purpleness' by the same central machinery
that makes purpleness out of redness from one eye and violetness from
the other. In the retina, then, there is some analytical mechanism, two
separate parts of which respond independently to the short and long
wavelengths in the purple light. We suppose the whole of this analytical
mechanism to be a group of (three) photochemical substances.

Left Eye

Right Eye Left Eye

I (none) I ■• — stimulus — - 1 red

i \ peripheral
\ \ analysis '

Right Eye

central synthesis -—>
binocular- mix lure locus
consciousness

Fig. 3 1 — Perception of a compound color : purple.

a, monocularly (or, a purple stimulus might be supplied to each eye), b, by binocular
mixture of red and violet. The inactive components of the visual system are labelled in
faint lettering — all components would of course be active in the perception of the all-
inclusive compound white.

Central Events in Trichromatic Vision — When the dark-adapted
eye is presented with an equal-energy spectrum, that spectrum appears
colorless (some say, faintly violet) but not homogeneous. At the locus
of wavelength 510m[X the spectrum is maximally bright, the luminosity
falling off toward the ends and becoming zero, at the long-wave end,
at a point corresponding to the orange-red of the photopic spectrum.
Konig and Trendelenburg, around the turn of the century, established

92 THE VISUAL PROCESS

between them the practical identity of this 'scotopic brightness curve'
with that of the photopic totally color-blind eye, the absorption spectrum
of rhodopsin, and the curve of the rhodopsin-bleaching power of mono-
chromatic lights (Fig. 33, c/. Fig. 35). The rods are completely insen-
sitive to deep red because rhodopsin absorbs nothing beyond X650mp,,
and they are most sensitive to green because this kind of light is more
avidly absorbed by rhodopsin than any other.

As the intensity of the spectrum is now increased, there is a range of
intensity — called the photochromatic interval — within which the spec-
trum remains colorless. This interval is not the same for all regions.
For red, it is of course non-existent, for as soon as wavelengths longer
than 650m|X are seen at all they are seen by cones, and are seen as red
light. In succession toward the violet end, the other hues appear as the
thresholds of the cones for them are crossed. The now fully colored
spectrum has its brightest part moved (the Purkinje shift) to around
A557m[X, and extends from A,390m^ to ^760m^l. Beyond A,650m|X lies
the pure red. At A,600m[l is orange. The exact center of yellow is at
A,582m^, of green at A,515m[X, of blue at A,476m[X. Beyond the indigo
of X424-455m[i lies the true violet (see Table I, p. 4).

In the neighborhood of yellow and blue the change in hue for a given
change in wavelength is greatest. To be exact, the two maxima lie at
A,580mp, and A,490m(l. Around these values, we can discriminate more
different hues, closer together in the spectrum, than we can elsewhere.
This is because these wavelengths are maxima in the graph of the in-
trinsic pallidity or tinsaturation of the spectrum: as we pass from one
side of such a maximum through it to the other side, the appearance of
the stimulus changes rapidly with a change in wavelength because the
ratio of chroma to whiteness in the sensation is changing so rapidly.

The blue maximum, and the minor peak of brightness in this region,
may be lowered somewhat by absorption in the yellow pigment of the
macula lutea of the retina (see Chapter 8, section D) . As the intensity
is raised however, yellow and blue stand out more and more. The hues
on either side of each of these actually change, gravitating toward which-
ever of the two is the nearer — that is, yellow and blue appear to spread
more widely in the spectrum at the expense of their neighbors, until at
very high intensities yellow and blue alone, greatly unsaturated, fill up
the whole spectrum. At dazzling intensities even these lose all chroma
and a sensation of whiteness is then evoked by any visible wavelength.

TRICHROMATIC VISION 93

Yellow and blue thus appear unique in some respect. We shall see
other aspects of their peculiarity shortly. It is important to note here
only the fact that hue can be influenced by intensity. Apparently when
the visual mechanism is being overworked, either its peripheral analytic
or its central synthetic portion breaks down. We can change the hues
that 'go with' particular wavelengths in still another way : by fatiguing
the reception of a part of the spectrum we can make white light appear
to consist only of the remainder of the spectrum, as in the production of
'complementary after-images'. More important, we can fatigue the syn-
thetic mechanism itself, for if we stare for a time at a light which repre-
sents white-minus-red, and then look into a spectroscope, we will see not
only the red where it 'belongs', but will see nearly the whole spectrum
as red; and where there is no red (at the short-wave end) there is only
darkness.* In the same way, green or violet can be made to spread out
and fill almost the entirety of the spectrum, but yellow and blue cannot
be made to do so. No better confirmation of our choice of red, green
and violet as primary stimuli could be desired.

This phenomenon shows beyond question that whatever the three
somethings may be which comprise the color-vision mechanism, each one
of them has some responsiveness for practically all visible wavelengths.
The results of fatiguing with colors show also that if each one of the
somethings could be isolated and made to act all alone, its action would
be to arouse a sensation of its appropriate primary hue, no matter what
wavelength of light happened to activate it. Most of the 160-odd sep-
arate qualities we can experience, then, must be due to the instigation,
by single wavelengths, of combined actions of the three processes, no one
of which alone could give us more than a single, primary, hue sensation.

A rough idea of these combined actions is given by Figure 32. Each of
the three colored curves represents the spectrum of responsiveness of one
of the three central processes which synthesize our hue qualities, and the
color of the line indicates the quality it arouses when allowed to act
singly. When the redness and green-ness processes are equally active,
the quality 'yellowness' results. When the green-ness and violet-ness

*The Ericksons have recently reported experiments which suggest that all 'fatiguing" for
color may be central, rather than upon a peripheral exhaustion-of-photochemicals basis.
Their hypnotized subjects 'saw' the proper complementary after-image colors after having
had hallucinatory initial color-stimuli suggested to them; and these were persons who, in
the waking state, did not know that there is such a thing as an after-image — let alone,
that it should be experted to be complementary to the stimulus!

94

THE VISUAL PROCESS

N0liVSN3S dO 3anilN9V^

TRICHROMATIC VISION 95

processes are equal, the resulting sensation is 'blue'. When all three are
equally activated (which of course cannot be brought about by any one
wavelength) 'white' results.

At any one wavelength the ordinate, or height of the curves, has a
heavy portion where it lies below all three curves. This represents equal
amounts of activity of all three processes, and so represents the white
valence, or unsaturating whiteness-component, of the sensation aroused
by that wavelength. It needs of course to be given triple weight in any
estimation of the relative whiteness- and chroma-contents of the various
color sensations — their degrees of saturation. Above the triple line, the
remainder of the ordinate represents chroma. The part of it which lies
under two curves, taken twice, represents equal joint action of the pro-
cesses represented by the two uppermost curves. At ?.582m(X for example,
the two uppermost curves cross and these processes are therefore equally
aroused, yielding the compound sensation of yellow, diluted by a great
deal of whiteness indicated by the heavy part of the ordinate lying
below all three curves. Near the ends of the spectrum all of the ordinate
represents chroma, which is another way of saying that these wave-
lengths are seen with complete saturation.

The unique character of yellow is now readily comprehensible from
the graph. It results from the equal action of two processes which singly
would yield respectively redness and green-ness, neither of which can
be seen in yellow. Blue has a similar mode of origin — it is the unpre-
dictable giraffe progeny of the horse of green and the zebra of violet.
All of the sensation-qualities of mixed character except yellow and blue
owe themselves to simpler blendings of sensation-components which, as
with purple and orange, can still be discerned in the blend. The very
names we use for mixed colors — bluish-red, reddish-yellow, and so forth
— emphasize the simple character of their mixtures. On the other hand,
no one would ever call yellow 'reddish-green', or blue 'greenish-violet' —
and yet, in their genesis, that is what they are.

Let us consider just one of these mixed colors whose whole is merely
the sum of its parts: orange. It will serve to exemplify the manner in
which all such mixed colors are registered. At wavelength 600m [i in
Figure 32, it will be seen that the double portion of the ordinate below
the curve of the green-process is only half as tall as the part between the
green and the red curves. But this part which is under the green curve
is under the red curve as well, and hence is to be 'taken twice'. More-
over, it represents equal contributions of redness and green-ness to the

96 THE VISUAL PROCESS

whole sensation aroused by X600m|i — that is, a certain amount of yellow-
ness. An equal amount of uncancelled redness still remains — the chroma
ordinate above the green curve, taken once as to weight in the equation.
At X600m|l, then, the interaction of the three processes produces a large
amount of whiteness and equal amounts of yellowness and redness. Such
a blend, we see as orange.

Before we leave Figure 32 its representation of relative brightness and
saturation need brief consideration. Brightness is most easily disposed
of — as the reader has already gathered, it is represented by the total
height of the variously-weighted portions of the ordinate. If each ordin-
ate were drawn upward like an unfolding telescope to its 'true' height,
the overall profile of the graph would represent exactly the curve of
brightness of the photopic spectrum.

Saturation is maximal (100%!) at the ends of the spectrum — a fact
which often goes unappreciated because of the low brightness of those
regions and the confusion of brightness and saturation in the mind of
the student. Saturation is always the degree of freedom from admixture
with white, whether white external to the source of color is objectively
added to the latter or not; for, the color itself, even if generated by a
single wavelength, contains unsaturating whiteness as long as the wave-
length in question sets off all three components of the central synthetic
mechanism to any extents whatever. Under all ordinary circumstances
we cannot have 'pure' colors, even in the spectroscope, without accepting
an adulteration thereof by whiteness which arises from causes entirely
within the central mechanism. In Figure 32, the intrinsic degree of satur-
ation of any wavelength can be seen as the ratio of total chroma to white-
ness, remembering to take singly the part of the ordinate from the top-
most curve to the next one down, doubly the portion from that curve
to the lowest, and triply the heavy line representing whiteness. It is
obvious, however, that by fatiguing with the complement of a color we
will so greatly reduce the height of the whiteness-ordinate that the satur-
ation of the color will be correspondingly increased. Fatiguing with
violet, for example, makes the yellow of the spectroscope — ordinarily
the least saturated of all its hues — become amazingly rich in chroma;
an experience never to be had otherwise, and never to be forgotten.

Color Blindness — 'Color blindness' is an unfortunate term which in-
cludes at least five, perhaps six, kinds of departure from the normal
trichromatic system. Total color blindness is the only type in which no

COLOR BLINDNESS 97

hues at all are seen, hence is the only type which should ever have been
called color blindness at all. Vision is restricted to white, grays, and
black, and the condition had best be called 'achromatic vision'. It seems
nearly always to be due to the congenital absence, or a gross defective-
ness, of the cones, for along with it there are usually to be seen : (a) low
visual acuity both scotopically and photopically; (b) a central scotoma or
blind spot where the bouquet of foveal cones should be ; (c) a nystagmus
or uncontrollable fluttering of the eyeballs owing to the lack of this cen-
tral fixating region; and (d) photophobia or light-shyness, owing perhaps
to an excess of rods, occupying the spaces where cones should be.

In 'anomalous trichromatic vision', some one spectral region appears
less bright than it does to the normal person, and the individual requires
more of such light, mixed with some other color, to match an inter-
mediate color. An individual who, say, perceives green weakly must mix
more green with less red than the normal individual, in order to match
a standard yellow. This condition is not color blindness — it would much
better be called color weakness.

These color-weak individuals have poor hue-discrimination and an in-
creased perception-time for colors. They fatigue rapidly for colors, which
seem to them to fade upon continued observation; and to identify some
colors they require them in larger areas, with greater intensity and satur-
ation, than the normal. Anomalous trichromates probably outnumber all
other kinds of so-called color-blinds, but since they less often get into
difficulty through unfortunate selections at the neckwear counter, they
usually live and die without ever knowing of their peculiarity.

The conspicuous and familiar color-blind type is the dichromate or
Daltonist, whose confusion of red and green is proverbial — and also
hereditary, in a sex-linked fashion which keeps the defect a rare one in
females. One white man in twenty-five is a dichromate, but only one
white woman in twenty-five hundred. The dichromate is so called because
he requires only two primaries, instead of three, to mix and match any
and all hues and white. It so happens also that he can experience only
two hues instead of the large number* of the normal trichromate; but
the prefix (di = two) on his label does not refer, to this latter fact. The
dichromate is not color-blind — he is color-poor.

^Usually taken as 160-180; but these are the discriminable hue-and-saturation complexes.
Similarly, a dichromate can distinguish a large number (about 60) of spectral regions, tut
chiefly through saturation-difrerences.

98 THE VISUAL PROCESS

The dichromate, in distinguishing most natural colors, must fall back
upon saturation- and brightness-differences. The former are much the
more important to him. Longwave colors look alike in hue to him, but
very different in saturation. It is widely supposed, even by some expert
psychologists, that a dichromate motorist tells red traffic signals from
green ones on a basis of brightness, and is helpless to do so when bad
weather dims them both. This is not the case. The brightness of the red
and green lights could be varied up or down, or the red light made much
brighter than the green (the reverse is usually true) without inverting
his identifications; for the two lights would still retain their very different
saturations.

For a long time, Daltonism was thought to be due to a literal absence
of one of the three sets of receptors, or photochemical substances, or
cerebral perceptual processes, of the Young-Helmholtz scheme of things.
It was the physiologist Fick who showed, many years ago, that this could
not be the explanation; but the lack-of-one-process theory is still taught
far and wide. To adjust Figure 32 to represent dichromatic vision in ac-
cordance with Fick's contributions, none of the colored curves should
be removed. It is only necessary to suppose that the spectrum of respon-
siveness of one of the three 'somethings' has shifted into coincidence
with that of one of the other two.

To be specific, let us suppose that the redness curve is altered so that
it superimposes upon the green-ness curve, and see what should inevit-
ably result in the vision of the individual. Firstly, the spectrum would
be shortened at the red end even in bright light. Secondly, redness and
green-ness would always be contributed equally to the sensation evoked
by all wavelengths from 650m[i to 476m[X. So, in this whole great spec-
tral region the individual could see only yellow with varying degrees of
saturation and brightness. He would have to learn to call the highly-
saturated wavelengths red, and to call the less saturated ones yellow or
green. Thirdly, from 7.476m[A on to the ultra-violet, only violetness
could be experienced, with saturation increasing as wavelength decreased.
But his spectrum would contain something besides yellow and violet;
for (fourthly) at X476m\i all three processes would be in action to the
same degree : white would result at this 'neutral point' in his spectrum.
Fifthly and lastly, purple would not exist for him, for since redness and
green-ness were inextricably tied together as yellowness in the long-
wave part of the spectrum, the mixture of any wavelengths there, even
those seen by the normal as red, with any of the wavelengths seen by

COLOR BLINDNESS 99

himself as 'violet', could yield only white since yellow and violet are
complementary. For such an individual, proper amounts of any two
wavelengths which were not on the same side of his neutral point could
be mixed as complementaries to make white.

Now, the above is actually a fair description of one kind of dichrom-
atic vision, called 'protanopia' in the older terminology since it was sup-
posed to result from the lack of the first (protos = first) of the three
component processes of trichromatic vision. Another, much more com-
mon, type is 'deuteranopia' (from deuteros = second) . This form we can
represent by shifting the green curve in Figure 32 to lie on top of the
red one. The deuteranope experiences no shortening of the spectrum at
the red end, and his neutral point is nearer the red end than that of the
protanope (though neither of the actual neutral points is quite where it
ought to be as theoretically called for by the diagram.) Otherwise, his
experiences are about the same : two hues only, with one at either side of
the neutral point; the same white region at the neutral point; and the
same white or gray sensations from stimuli which appear to the normal
as purple.

A condition much like dichromasy occurs, as a rarity, in one eye only.
The individual is then able to tell us what he sees with that eye in terms
of the trichromatic visual performance of his normal eye. Usually, he
reports that the spectrum contains only yellow and blue, not violet as
described above; but such pathological cases could not be expected to
duplicate perfectly the situation in true Daltonism.

Theoretically, two other kinds of dichromasy are possible, but only
one of them has been found (or else the two have been confused) :
'tritanopia' is so extremely rare that it has not had proper study. We
could represent its two possible versions by aligning the green curve of
Figure 32 with the violet, or the violet curve with the green one. The tri-
tanope's neutral point, depending, would then coincide with either the
protanopic or deuteranopic one. In the latter case, the spectrum would
be shortened at the violet end. In either case, the only possible hue-
experiences, it would seem, would be red and blue. The shortened spec-
trum of at least some tritanopes seems to have been noticed by the older
investigators and recognized in the common name of the condition,
*blue-blindness'. Tritanopia can be simulated in some individuals by ex-
cessive absorption of short-wave light in an abnormally rich macular
pigmentation (see Chapter 8, section D), or in an extremely yellow,
pre-cataractous lens; and also by the yellowing of vision in jaundice

100 THE VISUAL PROCESS

(usually ascribed to tinting of the vitreous by bilirubin — but E. Sachs
finds no such yellowing in icteric dogs; perhaps the retina is colored).

Photochemistry of Color Vision — So much as to suggestions re-
garding what goes on in the higher reaches of the chromatic visual
mechanism. Now, what objective realities can we point to, in the way
of a physiological mechanism for analyzing and transmitting assort-
ments of wavelengths in and from the eye? Sadly, only one dubious
photochemical substance of ambiguous properties.

In 1930, Gotthilft von Studnitz reported the first revelation of a
retinal photochemical since the discovery of Boll and Kiihne. Studnitz
has never given the material a real name — it is just the *Zapfensubstanz'
{i.e., cone-substance) . Several years later Wald in this country, without
reference to Studnitz's work, hypothesized a cone substance which he
named iodopsin (iodos = violet) on the assumption that if one could iso-
late and concentrate it, it would be found to be violet in color. 'Iodop-
sin', however, was based upon technical methods which Studnitz has ever
since insisted could not possibly have indicated his own zapfensubstanz,
but rather involved a serious error on Wald's part, Studnitz has con-
sequently refrained from applying Wald's appropriate name to the sub-
stance which he has claimed to be able to extract and study. For any
detailed discussion of the zapfensubstanz, the reader must go to the
work of Studnitz cited in the bibliography. No one outside of his group
has worked on the substance in all the years since its announcement.
Remarks on it here will be brief,

Studnitz first identified this photosensitive substance by comparing
the capacity of a fresh retina for absorbing light, before and after being
exposed to strong light. After such exposure, the retina was found to
be more transparent than before, which could apparently only be the
result of the destruction of some photosensitive substance. The first
retinae employed were duplex; so, to eliminate rhodopsin from the pic-
ture, Studnitz repeated his experiments on some pure-cone retinae. Here
also he found the substance, which therefore must be in the cones. He
learned how to study it by itself in rhodopsin-bearing retinae, though not
how to isolate its effects very well from those of cone oil-droplet pigments,
which come out in the same solvents and are slightly photosensitive.

By comparing the change, before and after the bleaching with strong
light, in the amount of various monochromatic lights absorbed, Studnitz
was enabled to plot a curve of the absorption spectrum of the zapfen-

PHOTOCHEMISTRY OF COLOR VISION

101

substanz; and this curve eventually received complete confirmation when
he obtained the absorption spectrum of the compound isolated from the
retina by extraction with ether and chloroform. Extracts of fish, frog,
turtle, and mammalian material contained various, always tiny, amounts
of the material whose maximum absorption of light was invariably at
A,560m|X or thereabouts — the position of the peak of the photopic bright-
ness curve, just as the peak of absorption of rhodopsin coincides with
the bright spot in the scotopic spectrum (Fig. 34; cf. Fig. 33).

In fact, the absorption spectrum of the zapfensubstanz proved to be
superimposible over the photopic brightness curve, after some alter-
ations which lay Studnitz open to the serious charge of 'wangling'.

^50

400

500 600

WAVELENGTH(mn)

Fig. 33 — Similarity of the graph of the
absorption spectrum of rhodopsin (frog)
and that of the luminosity of the spec-
trum to the scotopic human eye. Re-
drawn from Grundfest.

^'90
§80

(Teo

4(

500 600

WAVELENGTH(my)

Fig. 34 — Similarity of the graph of the sup-
posed absorption spectrum of the photochem-
ical material of the cones, and that of the
electrical responsivity of the photopic retina
through a portion of the photopic spearum
(here taken as indicative of photopic lumin-
osities). Redrawn from von Studnitz.

Herein lies the chief claim of the zapfensubstanz to acceptance as the
essential photochemical of cone vision — and, at the same time, its most
puzzling quality when the Young-He Imholtz theory is kept in mind.
It is very nice to hear at last that there really is an extractible photo-
chemical substance in the vertebrate cone visual cell. It is not so con-
venient to find that this one substance, single-handedly, appears capable
of accounting for the whole of the photopic brightness curve. There
ought to be three zapfensubstanzes, the overall profile of whose absorp-
tion spectra would just neatly fill out all the corners under that curve!
Studnitz, indeed, recognizes the possibility that what he has called one
substance is really a group of three which his solvents cannot separate
from each other. In fact his very latest curves, derived from snake

102

THE VISUAL PROCESS

material, show three peaks instead of one. He thinks the precursor of
the substance is the carotenoid pigment of the cones' oil-droplets (for
this there is no evidence whatever) and points out that the multiplicity
of such pigments in turtles and birds suggests that several different
photochemicals, a la the multi-component color-vision theories, are formed
from them. How this works out in the lizard, which sees all colors and
yet has only yellow pigment in its oil-droplets — or in man, who has no
oil-droplets at all (see Chapter 8, section D), Studnitz does not tell us.
So far, then, we are told of but the one substance. Its very existence
is most dubious, for leading authorities are very skeptical of Studnitz's

/ ,.' man, a .,
/^-photopic \\ \
scotopic— \\

owl, scotopic-

400 500 600 700

Wavelength (mp)

Fig. 35 — The Purkinje shift as shown
by the relative brightnesses of mono-
chromatic lights to the photopic and
scotopic human eye. Also, the relative
pupil -closing effectiveness of mono-
chromatic lights upon the scotopic
eye of an owl, Asia wilsonianus.
Redrawn from Hecht and Pirenne.

<08

I04

fish-.;'

'6g

t

12 m
h

Q
08-j-

600 550 500 450

Wavelength (mp)

Fig. 36 — Formation of acid (phosphoric?) in
retinje under monochromatic light — supposedly
owing to breakdown of the cones' photosensitive
material, and showing similarity to graphs of
photopic brightnesses. Redrawn from von Stud-

claims and critical of his methods. Granting that Studnitz has really
found a cone-substance — it may really be three, but if so we know not
how to separate them. Its precursor is quite unknown; but its end-
product upon breakdown under light is supposed to be phosphoric acid
(Fig. 36) . When we try to understand the retinal part of the physiology
of color vision, a single zapfensubstanz seems more of a hindrance than
a help. And if we choose rather to believe in the solitary 'iodopsin' of
Wald and Qiase, we are no better off. Different wavelengths would
break down different amounts of the whole concentration of the sub-
stance, and we can easily imagine that corresponding kinds of optic
nerve impulses — differing in modulation or whatnot — are produced and

PHOTOCHEMISTRY OF COLOR VISION 103

then integrated centrally where they set off the respective three com-
ponent processes of the synthetic mechanism. But, for any one wave-
length there is another on the other side of the peak of the absorption
spectrum of the zapfensubstanz, which at the same intensity would break
down the same amount of the substance into, presumably, the same end
products. How then could these two wavelengths possibly arouse differ-
ent sensations? It is impossible to imagine how any one substance could
serve as the analytical mechanism by which purple light is translated
into 'redness modulated' and Violet-ness modulated' impulses in a single
optic nerve fiber. For the cones to generate three qualitatively different
impulses, it would appear that they must contain a triplex photochemical
system.

In truth, the working out of the photochemical system of the cone
may long continue to seem the most difficult branch of the physiology
of the eye. To absorb more light in one part of the visible spectrum than
another, a substance must be colored. In the present state of our knowl-
edge we must suppose that there are tiny amounts of three differently-
colored photosensitive substances in the cone's outer segment. With the
very sloppiest of technique, we can mount the fresh dark-adapted retina
of a frog or a goldfish on the microscope and still see the rich wine of
rhodopsin filling its rods. But with the most careful of methods, we can
succeed in seeing living cones only as completely colorless structures,
whose bland innocence conceals invisible traces of three important some-
things— to our utter exasperation.

Chapter 5

THE GENESIS OF THE VERTEBRATE EYE

(A) Embryological

There are many anatomical relationships in the eye which are ex-
tremely puzzling when we look only at their adult condition, but which
become perfectly clear if we follow their ontogeny. A little knowledge
of the embryonic development of the eye is therefore highly desirable.
The process is a fascinating one in its own right, but we shall examine it
here as a means to two ends : the embryology of the eye can be expected
to shed some light upon its evolutionary origin; and, the developmental
scheme serves as a framework within which all possible adaptive evolu-
tionary changes of ocular structure must fit. If we know how the eye
develops we can guess where it came from, we can see how it has been
able to take on the modifications which fit it for greater efficiency in this
or that environment, and we can see why it has not been able to make
some changes that might seem to us more logical than particular ones
which it has happened to accomplish.

The following account is a generalized one which applies in its en-
tirety to no particular animal, but is based upon the mammals because
their story is known in the greatest detail. Some important departures
characteristic of other vertebrate classes will be pointed out specifically,
but in general the reader who wishes to imagine the ocular embryology
of a lower class needs only to make a mental subtraction, from the mam-
malian process, of those features which the lower group lacks, in order
to have a fairly accurate conception.

The parts of the eye are recruited from three sources in the embryo:
(a) the ectoderm of the neural tube, which is in turn derived by infold-
ing from the surface ectoderm and which later differentiates into the
brain and spinal cord; (b) the surface ectoderm remaining after the
neural tube has been formed and separated from it; and (c) the meso-
derm lying between the neural tube and the surface ectoderm.

Formation of the Optic Cup — These three sources start to make
their respective contributions in this same order. The brain being by far
the most complex organ in the body, it begins to develop before any
other; and the eye gets an equally precocious start since its most essen-

FORMATION OF THE OPTIC CUP 105

tial part, the retina, is a derivative of the neural tube. Even while the
tube is still an unclosed groove in the surface ectoderm, the beginnings
of the two retinae can be seen as a pair of dimples in the anterior portion
of its floor — the part destined to become the forebrain of the embryo.
As the lips of the neural groove approximate and fuse to close the
neural tube and push it beneath the surface ectoderm, these pits or
'foveolas opticas' (Fig. 37a) are each rotated through a right angle so
that they form a pair of bumps on the sides of the closed-in forebrain
(Fig. 37b). They rapidly expand as if blown up from the inside, and
each becomes a bubble of tissue attached to the side wall of the fore-
brain by a broad, very short, hollow stalk.

Fig. 37 — Formation of the optic vesicles.

a, cross section of anterior portion of frog neural groove, as yet unclosed, showing foveolie
opticce. Redrawn from Eyclesheimer.

b, cross section of head of 4mm. human embryo, after closure of the neural groove — the
foveolae now form the optic vesicles. Redrawn from Mann.

/- foveolae opticEc; fb- embryonic forebrain; m- mesoderm; tie- neural ectoderm; /- optic
stalk; se- surface ectoderm; v- optic vesicle.

At this stage the bubble of forebrain tissue is in contact with the sur-
face ectoderm of the side of the head and is known as the optic vesicle,
its connection with the forebrain proper being called the optic stalk. The
stalk slowly shifts its root backward as the brain becomes serially con-
stricted into five chambers, and is eventually connected with the second
of these, the diencephalon or tween-brain.

Two processes now set in, one in the optic vesicle and one in the
surface ectoderm, which go on simultaneously and look superficially as
though one of them must be causing the other : an indentation of the
optic vesicle to form a two-layered optic cup; and an in-sinking of a
portion of the surface ectoderm to form a closed hollow ball of tissue,
the lens vesicle, which comes to lie in the cavity of the optic cup. The

106

THE GENESIS OF THE VERTEBRATE EYE

formation of the lens vesicle is absolutely dependent upon the presence
of the optic vesicle against the surface ectoderm — but not in any
mechanical way: the lens-organizing influence of the optic vesicle is
exerted chemically. If the optic vesicle is removed, no lens vesicle is

Fig. 38 — Formation of the optic cup.

a, b, c, diagrammatic models of optic vesicle, transitional stage, and completed cup as seen
from the side of the embryonic head with the surface ectoderm removed. The curved arrows
in b show the direction of growth of the lateral portions of the vesicle which, while the
indentation of the face of the vesicle is taking place, grow below the level of the axis of the
optic stalk (dotted line) to form the ventral half of the cup. The embryonic fissure is
created by the temporary failure of the down-growing lobes to meet and fuse.

a', b', c', optical sections through the stalk axis (dotted line), corresponding respectively
to a, b, and c. A patch of surface eaoderm has been left in place to show the development
of the lens vesicle.

ef- embryonic fissure of optic cup; g- groove on underside of optic stalk (continuation of
embryonic fissure); i- invagination of face of vesicle; il- inner layer of optic cup (future
retina); Ip- lens placode; h- lens vesicle; ol- outer layer of optic cup (future pigment
epithelium); s- stalk; se- surface ectoderm.

formed; and if the optic vesicle is planted under any other surface ecto-
derm, even on the belly of the embryo, a lens vesicle will proceed to
form from that ectoderm. Similarly, if the developing lens vesicle is
removed, the optic vesicle goes right ahead with its indentation — the
latter is an active process, not caused mechanically by the inward pres-

FORMATION OF THE OPTIC CUP

107

sure of the developing lens; nor is the surface ectoderm passively sucked
inward, to form the lens vesicle, by the cupping of the optic vesicle.

The conversion of the optic vesicle into the optic cup is more than
a simple indentation or invagination (Fig. 38). At first, the dilated
vesicle lies largely above the level of the optic stalk, but after the com-
pletion of the optic cup the stalk is found to be attached to the center
of its back. Figure 38b shows what really happens — a growth of the two
sides of the base of the vesicle laterally and downward, closing in below
the attachment of the stalk. The closure is not at first complete, so that
a slit, the 'embryonic fissure of the optic cup' is left in the ventral

Fig. 39 — Cell-lineage
of the retina. Modified
from Fiirst. At the extreme
left is the initial coluninar-epithel-
ioid condition of the inner layer of
the optic cup. Germinative cells, occupy-
ing a position comparable to that of the
ependymal cells of the brain wall, proliferate a
pseudo-stratified tissue, some of whose elements
eventually retract one or both of the processes con-
necting their cell-bodies with the limiting surfaces. The ••*" -^lJ^::^^ /7
oldest, most vitread of the elements (bottom-most in the drawings) are about the first to
differentiate, and maturation proceeds outward toward the germinative cells, which at last
become the rods and cones.

r- portion of rod; c- cone; h- horizontal cell; m- Miiller fiber; b, b- bipolar neurons;

a- amacrine cell; g- body of ganglion cell; n- nerve fiber (axon of ganglion cell).

meridian of the cup, running from its rim to the cup end of the optic
stalk. Along the under side of the stalk, nearly all the way to the brain
wall, there is now a deep groove which has invaginated during the form-
ation of the optic cup. This groove opens into the cavity of the optic
cup and here forms the apex of the embryonic fissure. The old cavity
of the optic vesicle has been nearly obliterated by the indentation of the
vesicle. It, through its continuation in the optic stalk, still opens into
the forebrain cavity but of course has no communication with the new
cavity of the optic cup or with that cavity's continuation, the ventral
groove of the optic stalk.

108 THE GENESIS OF THE VERTEBRATE EYE

Differentiation of the Retina — The optic cup now has two layers
of tissue in its wall whereas the optic vesicle had but one (Fig. 38c', il,
ol) . The outermost of these layers remains forever one cell thick and its
cells shortly develop pigment granules, the whole layer becoming even-
tually the pigment epithelium of the retina. The cells of the inner layer
of the optic cup rapidly proliferate, forming many layers from which
will be derived the various layers of the adult sensory retina (Fig, 39).
Since it is the outermost of these cells (toward the pigment epithelium)
which are multiplying, their daughter cells are pushed ever inward
toward the cavity of the optic cup. It follows that these innermost cells
are the oldest at any one time and they are naturally the first to differ-
entiate. They lie in the position of the ganglion cells of the adult retina;
and it is into these that they develop, soon protruding their axon fibers
which grow along the inner surface of the optic cup. These fibers all
aim for the cup end of the optic stalk — the site of the future disc — and
here turn outward and grow down through the tissue of the stalk {not
through the groove on its under side) to make their connections in the
wall of the diencephalon. They form the optic nerve fibers; and a few
cells of the stalk tissue, which escape destruction by them, proliferate
the neuroglial cells which help to form the system of interfascicular
septa in the adult nerve.

The further differentiation of the cells of the inner layer of the optic
cup proceeds in a two-fold manner: from the inner surface toward the
outer (next the pigment epithelium) and from the posterior pole of the
cup forward along all meridians toward the rim. At the posterior pole,
the future amacrine cells can be recognized soon after the ganglion cells
and Miiller fibers have differentiated. The bipolars and horizontal cells
next become distinguishable; and, when proliferation finally ceases, the
cells nearest the pigment epithelium (which have been doing the pro-
liferating) are finally free to differentiate into the rods and cones — the
last elements in the retina to mature though they are the most ancient
cells in the eye and are its whole reason for being.

At any one time, these changes are further advanced at the posterior
pole than they are out toward the rim of the cup, where cell-division
may still be seen long after it has ceased in the fundus of the retina.
The optic cup thus grows at its lip, and rapidly increases manyfold in
diameter and in surface area as the embryo enlarges. A convenient con-
sequence of this is that it is possible to study the whole process of retinal
differentiation in a single favorable section of a single embryonic eye,

DIFFERENTIATION OF RETINA; LENS 109

simply by examining regions which are successively farther from the
posterior pole and nearer to the ora terminalis, or rim of the cup. An-
other consequence is that the region of the ora is to some extent perma-
nently juvenile. If the retina is destroyed and subsequently regenerates
(as it will do in amphibians, though not in any other vertebrates) the
new retina grows from the ora terminalis, creeping backward until the
fundus is filled; and a new optic nerve develops pari passu with the
regeneration. A perennial mystery, however, is the fact that the retina
continues to increase greatly in extent after all cell-division has appar-
ently ceased in it — as is the case, for instance, in an amphibian which is
on the verge of metamorphosis, though the eye is then nowhere nearly
adult in size. It is possible that sensory-retinal elements continue to
differentiate from the ciliary epithelial cells (v.i.) at the ora, and the
application of the colchicine technique may solve this problem.

The Lens — All this time, the lens has been developing. Commencing
as a local thickening in the surface ectoderm, the 'lens placode' evoked
by some chemical emanation from the contiguous optic vesicle, it has
invaginated and pinched free of the surface ectoderm, which heals over
it without trace.

Thus is formed the lens vesicle, lying in the mouth of the optic cup
(Fig. 38c'). Its posterior or inner wall rapidly thickens, each of the
cuboidal cells becoming columnar and continuing to elongate until it
is a slender fiber. The growth in length of these cells being in a forward
direction, they encroach upon the cavity of the lens vesicle and oblit-
erate it, forming a solid mass whose anterior surface is still covered over
by the unmodified cuboidal cells of the original anterior wall of the
vesicle (Fig. 40). This cuboidal layer is the lens epithelium, and at the
equator of the lens it forever remains continuous with the greatly thick-
ened posterior wall. In this region of transition, epithelial cells now
commence to elongate and to rotate their axes of polarity until they are
no longer radially oriented with respect to the center of the lens, but
circumferentially disposed (Fig. 41a). The two ends of these elongating
equatorial cells disconnect from the ends of their neighbors in the epi-
thelium and grow apace, one end sliding forward under the epithelium
and the other end backward, guided by the confining capsule which has
already been secreted by the lens vesicle over its whole outer surface.

Thus a layer of circumferential lens fibers is laid down, like one of
the skins of an onion, over the central mass of original, straight lens

110

THE GENESIS OF THE VERTEBRATE EYE

fibers which were formed directly from the cells of the posterior wall of
the lens vesicle. The further conversion of crop after crop of cuboidal
epithelial cells, at the equator of the lens, results in layer after layer of
fibers each of which is added outside of the previous one (Fig. 41b).
Any one fiber being too short to stretch from pole to pole of the lens,
its anterior and posterior ends meet, head-on, the corresponding ends

Fig. 40 — Early stages of the lens. Redrawn from Mann.

a, placode stage, comparable with Figure 38a'; p- lens placode formed in surface ectoderm;
ov- optic vesicle, b, c, lens pit forming and closing off; cl- lips of optic cup. d, lens vesicle
has detached and passed into mouth of optic cup; Iv- lens vesicle; m- mesenchyme which has
now invaded space between optic cup and surface ertoderm. e, cavity of lens vesicle being
obliterated by the elongation of the posterior wall cells to form the first of the lens fibers.
f, lens is now solid, and its present fiber mass will constitute the 'embryonic nucleus' of
later life (cf. Fig. 41b); ^ zone of transition of epithelium into fibers — the locus at which
all future fibers will form; ac- anterior chamber forming as a cleft in the mesoderm, separ-
ating the latter into the future cornea and the future iris stroma, g, new fibers have been
added to the embryonic nucleus and are meeting end-to-end at anterior and posterior suture
planes; s- posterior suture {cf. Fig. 41b, sp).

of a diametrically opposite fiber. These meeting points are aligned in
radial planes within the lens mass, called lens sutures (Figs. 40g, 41b
and c) , which perforce branch more and more toward the surface of the
growing lens as the number of epithelial cells ringing the equator in-
creases and the number of fibers seeking place for their tips against the
suture planes increases. At any one time, there are many superficial
layers in which the fibers have not yet elongated enough to reach suture

Fig. 41— Growth of the lens.

a, diagram of the equatorial region of a growing lens, showing how the cells of the lens
epithelium, e, elongate and reorient their axes of polarity to convert into lens fibers, /, whose
ends slide forward under the epithelium and backward under the capsule, c, as they take
on a circumferential course.

b, diagram showing growth of lens fibers; the youngest, in the vicinity of /, are still in
contact with the epithelium e and capsule c (c/. a). /'- cortical fibers which are still grow-
ing as indicated by the arrows, and have not yet reached suture planes. Their nuclei,
distributed along the nuclear bow nb, slowly fade as the fibers gradually sclerose upon being
marooned in the heart of the lens by the addition of newer fibers peripheral to them.
Oldest, hardest fibers of all are those of the 'embryonic nucleus' en, formed direaly from
the posterior wall of the lens vesicle (c/. Fig. 40). /"- fibers which have reached the suture
plane sp. (All fibers in the section are shown as if in one plane — aaually, they spiral so
that the suture planes of the front and back halves of the lens are at right angles; c/. c).

c, superficial fibers of the adolescent nucleus of the human lens, showing the 'lens stars'
which represent the intersections of the branched suture planes with the surface. Redrawn
from Mann.

d, portion of equatorial section of human lens, showing radial lamellae of lens fibers and the
hexagonal shape of the latter in cross seaion. x 500. From Maximow and Bloom, after
Schaffer. b- branching of a radial lamella, which occurs repeatedly as the equatorial peri-
meter of the lens enlarges during growth. (All the fibers shown in a lie in one radial lamella).

Ill

112

THE GENESIS OF THE VERTEBRATE EYE

planes, creating an unsutured cortex overlying a sutured core, the cortex
becoming proportionately thinner as the lens ages and the rate of fiber-
formation is slowed (see also pp. 20-1).

Fig. 42 — The hyaloid circulation.

a, model of invaginating mammalian optic vesicle, showing future hyaloid artery being taken
up through the embryonic fissure. Based upon figures of Mann.

bw- brain wall; ca- carotid artery; cv- first chonoidal vessels, which will anastamose around
cup rim to form the annular vessel, and will branch over cup surface to lay down the
choriocapillaris; ha- hyaloid artery.

b, model of fetal mammalian eye in optical section, showing the hyaloid system at the peak
of its development. Based upon figures of Versari.

ac- anterior chamber; av- annular vessel; hp- Bergmeister's papilla (neuroglial support at
base of hyaloid, which will later atrophy with the hyaloid vessels, leaving a cup in the
nerve head); c- cornea; cc- choriocapillaris (first vessels of the chorioid to form); Ad-
trunk of hyaloid artery, traversing vitreous cavity; im- ins mesoderm, containing capillary
arcades thrown forward from annular vessel; /- lens; mc- mesenchymal (mesodermal) con-
densation which will form chorioid and sclera; p- lids (temporarily fused over cornea);
pe- pigment epithelium of retina; r- retina, with neuroblastic layer still single anteriorly
but already divided into inner and outer layers in the precocious fundal region; tvl- vessels
of tunica vasculosa lentis, encapsulating the growing lens; vhp- vasa hyaloidea propria,
supplymg the vitreous and the retinal surface — the last vessels of the system to differ-
entiate, and usually the first to atrophy.

This growth process never completely stops until death, though it is
greatly retarded after the eye has reached its adult size. The oldest fibers
of the lens being the innermost ones, it is these which first feel the effects
of being removed farther and farther from any possible source of food
and oxygen, and they sclerose (harden) and die. The sclerosis involves

HYALOID CIRCULATION; VITREOUS 113

more and more outlying layers of fibers until the dead, firm centrum of
the lens has grown in size (by middle age) to the point where little
accommodatory change of shape of the lens is any longer possible (see
Fig. 15, p. 35). The lens is thus unique among the organs of the body
in that its development never ceases, while its senescence commences
even before birth.

The Hyaloid Circulation — In mammals, though not in any other
class, the developing lens is nourished by an elaborate temporary net-
work of blood vessels. The first signs of their development are seen while
the optic cup is just being formed. From a plexus of embryonic capil-
laries lying beneath the vesicle, one especially plump vessel is taken up
into the groove of the optic stalk (Fig. 42a) so that when the lips of this
groove finally close, the little vessel lies along the axis of the future optic
nerve and forms the 'hyaloid artery'. At the optic-cup end of the groove
of the optic stalk, it emerges into the cup cavity. The healing of the
embryonic fissure of the optic cup fixes the point of emergence of the
hyaloid artery at the site of the apex of the fissure. As it traverses the
vitreous cavity it branches around the lens to form a vascular tunic on
the latter, and some of these branches make connections at the rim of the
optic cup with other vessels clinging to the outer surface of the cup, the
beginnings of the chorioidal circulation. A ring-shaped 'annular vessel'
is formed at the cup margin, and from it capillary loops are thrown over
the anterior face of the lens, budding through the mesodermal tissue
which has squeezed in between the lens and the surface ectoderm, and
thus laying down the circulation of the embryonic iris (Fig. 42b).

The whole vascular net around the lens, the other branches of the
hyaloid artery which run along the inner surface of the retina, and
the hyaloid artery itself eventually (before birth) atrophy back to the
head of the optic nerve. Here the hyaloid (now called the central
retinal artery) gives off new branches into the retinal tissue, accom-
panied by branches of the central retinal vein, to give the retina its
definitive circulation.

The Vitreous — In among these temporary vessels in the cavity of the
young optic cup there is a gelatinous tissue, the 'primary vitreous', whose
few fibers are of dual origin, some being produced by mesodermal cells
which invaded the cup with the hyaloid vessel, others coming from the
foot-plates of the Miiller fibers of the developing retina, and even from
the cells of the lens until the formation of the capsule shuts off further

114 THE GENESIS OF THE VERTEBRATE EYE

contributions. Most of the definitive or secondary vitreous is secreted
by the retina during the growth of the eye, the primary vitreous coming
to form a slender cone with its base on the back of the lens and its apex
at the head of the optic nerve (Fig. 43). The final disappearance, from
this primary vitreous, of the last remnants of the hyaloid circulation
leaves it in the form of a conical tube (filled with vitreous thinner than

Fig. 43 — Formation of the vitreous.

a, diagrammatic section of young optic cup showing vessels of the hyaloid system embedded
in the primary vitreous, consisting of mesodermal fibers and cells (which invaded the cup
along with the hyaloid artery ha), together with fibrils secreted by the ectoderm of the cup,
lens, and surface.

b, diagrammatic section of fetal optic cup in which atrophy of the vasa hyaloidea propria
(c/. Fig. 42b) has clarified the peripheral vitreous, to which has now been added much
secondary vitreous (vertical hatching) secreted by the sensory retina. The persisting tunica
vasculosa lentis and the trunk of the hyaloid artery ha are embedded in a cone of primary
vitreous.

c, the definitive situation (c/. Fig. 3, p, 7): the canal of Cloquet represents the remnants
of the primary vitreous, stretched to a slender column by the growth of the eye (diagonal
hatching). The secondary vitreous (vertical hatching) nearly fills the globe. The tertiary
vitreous (horizontal hatching) is constituted by the fibers of the zonule, secreted lastly by
the non-sensory retina. The optic-nerve portion of the hyaloid artery alone persists, as the
central retinal artery era, and has given off new branches into the retinal tissue.

the secondary kind) , the canal of Cloquet. This canal runs through the
vitreous from disc to lens in the adult, with a considerable sag along
its course caused by gravity and time (see Fig. 3, p. 7).

The Vascular and Fibrous Tunics — As soon as pigment granules
appear in the outer layer of the finished optic cup, a network of capil-
laries— the future choriocapillaris — is formed in the mesoderm against
the pigment epithelium. Larger vessels developing outside of these, and

VASCULAR AND FIBROUS TUNICS

Fig. 44 — Formation of the anterior segment (modeled in optical seaion, based
upon the process in primates; scale decreases from a to d).

a, young embryo (cf. Fig. 40f). Anterior chamber has formed; lids closing over cornea;
scleral condensation has appeared.

b, advanced embryo. Chamber is broader; lids are fused by epithelial plug; cornea has
stratified epithelium, mesothelial lining; back wall of chamber still wholly mesodermal, but
optic cup margin has put forth a thin outgrowth bearing meridional ridges (ciliary pro-
cesses); major circle of iris can be made out.

c, fetus. Chamber still broader, its margin nearer to major circle; lids still fused but with
lash follicles. Meibomian and other glands budding in from ertoderm; Descemet's membrane
and canal of Schlemm formed; ciliary muscle and large-vessel layer of chorioid taking shape;
hyaloid system has degenerated; continued forward growth of optic cup margin (leaving
corona ciliaris behind) has given the iris mesoderm its ectodermal backing (from which the
sphinaer is differentiating) but leaves a thin film of mesoderm over the lens — the pupillary
membrane, which will soon atrophy.

d, fetus near term. Chamber will broaden yet more, well past Schlemm's canal; lids re-
opened and well differentiated; cornea and anterior sclera fibrous; reaus muscles formed;
ciliary muscle fully developed; iris complete — dilatator differentiated, pupillary membrane
gone; formerly narrow zone between original optic cup margin and precociously-formed
corona now greatly expanded, creating orbiculus ciliaris and leaving old cup margin far
behind as the ora terminalis; zonule fibers, growing out from orbiculus, have attached to
lens capsule.

ir- inferior rectus; //- lower lid; ot- ora terminalis; sr- superior rectus; «/- upper lid; zf-
zonule fibers.

116 THE GENESIS OF THE VERTEBRATE EYE

connected with them, become the arteries and veins of the chorioid coat.
The mesoderm around the optic cup condenses to form the connective-
tissue substrate of the chorioid and sclera, at first one mass but later
separated by the formation of the epichorioidal lymph-spaces. Other
early mesodermal condensations develop into the extra-ocular muscles
and other orbital contents.

The anterior chamber is formed quite early as a cleft in the mesoderm
between the lens and the surface ectoderm, separating this mesoderm
into that of the iris and that of the cornea (Fig. 40, ac; Fig. 44). The
two layers may become neat and regular even before their separation.
The corneal mesoderm differentiates into the substantia propria, and the
overlying surface ectoderm contributes the corneal epithelium. The
lining cells of the embryonic anterior chamber become the latter's meso-
thelium, secreting (on the inner side of the cornea) Descemet's mem-
brane as their basement membrane.

The iris is thus at first wholly mesodermal, and there is no aperture
in it, the future pupil being filled in by a mesodermal 'pupillary mem-
brane' which must later atrophy. The two ectodermal layers of epi-
thelium on the posterior surface of the iris are laid down by the optic
cup in the following way :

The thick rim of the optic cup, the future ora terminalis of the sensory
retina, suddenly resumes proliferation, and a bud-like prolongation of
it creeps out under the mesoderm of the iris, between that mesoderm
and the lens, forming a thin double epithelium whose two layers are
respective continuations of the pigment epithelium and the retina proper.
This is actually new growth, for the optic cup proper does not expand
to accomplish it, as is evidenced by the fact that the original thick rim
'stays put'. The first structure laid down by this thin anterior continu-
ation of the cup lip is the future corona ciliaris; but when this has been
produced the growing lip does not stop, but cuts through the vitreous
which is joined to the root of the iris and continues out under the iridic
mesoderm as far as the site of the future pupil margin, leaving the
pupillary membrane devoid of an ectodermal backing.

The outer layer of this epithelial fold is pigmented like the retinal
pigment epithelium of which it is a continuation, and during its growth
the pigmentation begins also to involve the inner layer of cells, creeping
backward from the growing lip as far as the root of the iris, where it
stops. This leaves the innermost of the two layers of epithelium which
cover the ciliary body forever free of pigment granules, forming the

LIDS AND GLANDS; NON-MAMMALS 117

ciliary epithelium. In the iris, the outer or anteriormost of the two layers
of epithelial cells eventually loses much of its pigment icf. Fig. 7g, p.
15) as it gives rise to the sphincter and dilatator of the pupil, which
are thus the only ectodermal muscles in the body.

In the ciliary body, mesodermal cells differentiate into the ciliary
muscle fibers, and the anterior chamber widens and deepens greatly
through the erosion of tissue at the iris angle. From the ciliary epithelium
there develop the cuticular fibers of the suspensory ligament or zonule,
which are regarded collectively as the tertiary vitreous and which grow
axiad to gain secondary attachments to the lens capsule. The anterior
surface of the secondary vitreous then drops back to its definitive posi-
tion, its surface presented to the aqueous forming the anterior hyaloid
membrane; and the aqueous of the anterior chamber is free to spread
back into the posterior chamber and the canal of Hannover. With the
formation of the zonule, the main features of the eyeball are established.

Lids and Glands — The lids arise as a circular fold of skin around the
front of the eye which closes in over the cornea, with its circular aper-
ture rapidly becoming a horizontal slit, thereby creating upper and
lower lids. The margins of these fuse together early in fetal life, opening
again much later — from a few days to six weeks after birth in mammals
which are born hairless and helpless. The time of reopening always
coincides closely with that at which the rods and cones have finished
their differentiation. That differentiation, it is interesting to note, can
be speeded up a couple of hundred percent by surgically opening the
lids of the newborn mammal and keeping it and its mother in a lighted
place. The various glands of the lids, the lacrimal and Harderian glands,
and the lacrimal drainage system are all ectodermal derivatives; but
their mode of development is unimportant to us here.

Variations in Non-Mammals — Some major departures from the
above process, which occur in the different vertebrate groups, are men-
tioned briefly below and will be dealt with at some length subsequently,
in appropriate places. Others will be self-evident to the reader when, in
later chapters, he encounters mention of the loss or gain of some feature
by one group of animals or another.

Lampreys : The epidermis and dermis of the skin are never fused to
the cornea to contribute respectively a corneal epithelium and a part
of the substantia propria. A patch of visual cells is already functional
in the primary optic vesicle (see Fig. 54c, p. 126) and persists as 'Retina

118 THE GENESIS OF THE VERTEBRATE EYE

A' in the growing eye until metamorphosis, when throughout the re-
mainder of the much-expanded retina ('Retina B') the visual cells are
suddenly differentiated and the borders of Retina A become indistin-
guishable. Retina A goes out of function when the tiny larva first bur-
rows into the mud, and the eye is blind until metamorphosis, when the
skin covering it becomes transparent and Retina B matures. No intra-
ocular muscles or suspensory-ligament fibers ever develop, for the pupil
is motionless and there is no ciliary body interposed between chorioid
and iris. The lens is propped in place only by the vitreous, which seems
to have evolved its semi-solid nature for this original purpose.

Fishes : Except in the elasmobranchs, the optic vesicle is at first solid
as is the central nervous system, both eye and brain becoming hollow
secondarily. In many of the bony fishes the embryonic fissure never quite
closes, and the chorioid erupts through it to form the 'falciform process'.
Others develop, instead, a network of vessels at the vitreo-retinal inter-
face. Those species which have a pseudobranch develop a huge capillary
mass in the chorioid, the 'chorioid gland'. True lids and associated
glands are usually lacking, though vertical, so-called 'adipose' lids are
common.

Amphibians: The fusion of the skin with the purely mesodermal,
inner layers of the cornea (those continuous with the sclera) is deferred
until metamorphosis, as is the development of the lids. The growing
suspensory-ligament fibers do not obliterate the anterior part of the
secondary vitreous, but remain embedded in it so that no aqueous-filled
cavities are ever formed behind the iris. Despite their entanglement, the
tertiary vitreous fibers are derived only from the ciliary epithelium, the
secondary vitreous solely from the sensory retina, just as in other verte-
brates.

Reptiles and Birds: The neuroglial supporting tissue of the head of
the optic nerve usually proliferates a vascular, pigmented 'pecten' pro-
jecting through the vitreous toward the lens. In birds the elongated
base of the pecten follows the course of the embryonic fissure, developing
from its lips. In some groups, an anterior portion of the embryonic
fissure never closes, and a meridional slit is thus left in the ventral part
of the ciliary body, through which the anterior and posterior chambers
communicate. The third eyelid or nictitating membrane (present also,
as the 'haw', in many mammals) arises as a vertical fold of conjunctiva
at the nasal side of the eye, covered by the upper and lower lids. The
equator of the lens and the ciliary body come into contact and remain

EVOLUTION OF EYE FROM BRAIN 119

SO (whereas in mammals they later separate, owing to the eye's growing
faster than the lens, so that the suspensory ligament is thereby put in a
state of tension, forcing the lens to become flatter during its growth).
In the snakes, the course of development of many parts has been pro-
foundly modified, as is explained in detail in section D of Chapter 16.

(B) Evolutionary

In its simplest terms as seen in the lamprey, the vertebrate eye has
only a very few essential living parts: retina, uvea, fibrous tunic, and
lens. The problem of the origin of the eye is merely the problem of the
status of each of these parts previous to their present association. Yet
though when thus stated the matter appears simple, it has baffled a great
many astute morphologists. The great German anatomist Froriep once
likened the 'sudden' appearance of the vertebrate eye in evolution to the
birth of Athena, full-grown and fully-armed, from the brow of Zeus.

The Eye a 'Part of the Brain' — From the embryology of the eye it
appears that there could have been no complex retina until the chordates
had evolved an internal, tubular brain. The foveolae opticae have been
interpreted as an ancestral stage in which the eyes were essentially a pair
of photosensory epithelial pits in the skin, analogous to those of a
modem Nautilus. Another possibility is that the foveolae are develop-
mental precocities without phylogenetic meaning. Before we can decide
how to interpret them, we shall have to try to determine how far back
the rods and cones may have been photosensory.

If the retina is thought of as a photosensory portion of the brain wall,
outpocketed to keep it near the skin in an ancestor whose body was
becoming larger and more opaque as evolution proceeded, then the scle-
rotic and uveal coats are easily disposed of by homologizing them with
the meningeal envelopes of the central nervous system, the dura mater
and the pia-arachnoid. The sclera is actually continuous with the dura
via the sheath of the optic nerve. The latter also possesses a continuation
of the pia-arachnoid, though this ends outside the eyeball and does not
merge with the chorioid even in the embryo. The vascularity and pig-
mentation of the chorioid are however strongly pia-like characteristics,
and in lampreys there are even striking histological similarities between
chorioid and pia.

120

THE GENESIS OF THE VERTEBRATE EYE

The big difficulties which an eye-origin theory must hurdle are: (a)
the inversion of the retina — the fact that the vertebrate visual cells point
away from the light; (b) the nature of the visual cells before they be-
come photosensory, and the question of their location at the time they
did so; and (c) the question of the status of the lens before it became
associated with the retina as a dioptric structure.

i^"^#il -*- inf

Fig. 45 — Sagittal section of 'brain' of Amphioxus.

(In the position it normally has in the living animal in its burrow). From Walls, after Franz.

aps- anterior pigment spot; dc- two of the dorsal cells of Joseph; inf- infundibular organ,
whose photosensory elements are flagellated ependymal cells.

Early Theories — Between 1874 and 1929 a series of investigators saw
the beginnings of the vertebrate eye in the anterior pigment ^ot of
Amphioxus (Fig. 45, aps). Even by 1890, however, experiments had
indicated that this 'eye' is not sensory at all, and at the present time
this is considered certain.

EARLY THEORIES

121

Lankester, in 1880, suggested that the eye of the vertebrate is com-
parable with that of the 'tadpole' larva of certain of the lower chordates,
the Ascidia. Others interpreted this suggestion as one of true homology,
and a debate sprang up over whether the ascidian eye was a degenerate

Fig. 46 — Illustrating the ascidian theory as originally conceived.

(At a time when the ascidian lens was mistakenly believed to lie toward the brain cavity).
From Walls, after Jelgersma.

a, ascidian eye, consisting of a retinal evagination of the brain wall and an internal lens, //.

b, hypothetical transitional stage in which two lenses were present, one on either side of
the retina.

c, vertebrate retina and definitive, 'outer' lens, derived from skin.

Fig. 47 — Illustrating Balfour's theory. From Walls, after Parker.

Patches of photosensory cells are shown in the successive positions which they are supposed
to have occupied before and after the evolution of the neural tube and the retinal evagin-
ations thereof.

offshoot of the vertebrate organ or a primitive fore-runner thereof. Froriep
later decided that neither of these views could be true, for the retina of
the ascidian eye is not inverted; but he thought that both eyes might
have had common ancestry in a pair of dermal eyes (Figs. 46 and 48).

122

THE GENESIS OF THE VERTEBRATE EYE

Balfour's Theory — It was Balfour, in 1881, who first proposed that
the vertebrate retina originated in the skin and was carried inside the
animal by the evolution of the neural tube (Fig. 47). Several investi-
gators, independently of each other, soon pointed out how well the fove-

Fig. 48 — Illustrating Froriep's derivation of the ascidian and vertebrate eyes.
(From common-ancestral superficial vesicular eyes). After Walls.

a, b, c, d, stages in the evolution of the ascidian eyes, showing the degeneration of one
member of the pair.

a, b', c', d', stages in the evolution of the lateral eyes of vertebrates.

o\x Opticas fit into this hypothesis (Figs. 49 and 50). Balfour's theory-
was the first to account for the inversion of the retina, but it offered no
explanation of the lens. It has however been suggested that inversion was
no accident, but had to be brought about somehow if the highly meta-

BALFOUR'S THEORY

123

bolic rods and cones were to have an adequate blood supply (the chori-
oid) without this lying between them and the light and blurring the
image. Moreover, it must be remembered that we have no certainty
whatever that the chordate nervous system originated as a tube — the
lowest vertebrates, which should show the most primitive situation, de-
velop it as a solid cord and canalize it secondarily.

Fig. 49 — The foveolce opticae in relation to Balfour's theory. From Walls.

a, unclosed brain region of neural tube of frog embryo, showing the foveolce optica, /-/,
as patches of pigmented columnar cells (after Franz).

b, c, d, stages in the evolution of the eyes, based on the development of the foveolae into
the retincB (after Lange).

Fig. 50 — Illustrating Schimkewitsch's

version o

f Balfour's theory.

(Deriving the lateral eyes from one of several pairs of photosensory pits in the surface ecto-
derm, of which the foveolaa optica are the embryological counterparts). From Walls, after
Schimkewitsch.

124

THE GENESIS OF THE VERTEBRATE EYE

Fig. 51 — Illustrating the placode theory. From Walls, after Beraneck.

A vesicular eye derived from a lateral-line organ loses its photosensitivity and becomes the
definitive lens, while its ganglion becomes photosensory and is converted into the definitive
retina.

St

fs

/-^^/

Fig. 52 — Hesse's organs of the 'spinal cord' of Amphioxus. From Walls, after Hesse.

a, a single organ, consisting of a pigment cell and a photosensory ganglion cell, whose
'stiftchensaum', st, was believed by Boveri to be a cuticular struaure comparable with the
outer segment of a rod or cone.

b, cross section of nerve cord, showing various orientation of the organs (enabling the animal
to respond to the direction of light).

THE PLACODE THEORY; BOVERl'S THEORY

The Placode Theory — The origin of the lens was first explained by
Sharp in 1885. He regarded the lens as a modified lateral-line organ
which was, like those organs, a sensory ectodermal pit or bud. The
'placode theory', an extension of Sharp's original idea, proposes that
the lens was once the whole eye and that the present retina served as its
ganglion, eventually taking over the sensory function itself and releasing
the vesicular 'skin' eye to become a lens (Fig. 51). Fatal objections to
this interpretation of the retina arise from the utter absence of embry-

Fig. 53 — Illustrating Boveri's theory. From Walls, after Boveri.
The Hesse's organs become the visual and pigment-epithelial cells of the vertebrate retina.

©logical confirmation of any previous connection of retina and lens,
and from the lack of any evidence that a self-determining lens placode
exists at all as a morphological entity — it will be recalled that it is called
into existence ontogenetically solely by the chemical influence of the
optic cup. Nor does the placode theory account for inversion.

Boveri's Theory — Inversion was explained anew by Boveri in 1904,
in a theory that made use of the two-celled visual organs of Amphioxus,
which had been discovered by Hesse in the 'spinal cord' of this so-called
grandfather of the vertebrates (Figs. 52 and 53). While Boveri's theory

126

THE GENESIS OF THE VERTEBRATE EYE

offers no account of the lens, it gives as good an explanation of the retina
and its inversion as does Balfour's theory; and both hypotheses are widely
taught at the present time. Acceptance of either is impossible, however,
unless the mode of development of the rods and cones indicates either
that they might have been already photosensory while still in the skin.

Fig. 54 — Illustrating Studnicka's theory. From Walls, after Studnicka.

The sensory cells of the median and lateral vertebrate eyes are derived from the flagellated
ependymal cells which line the neural tube, c represents the larval lamprey, in which the
eye is temporarily functional though the retina ('Retina A' — see p. 117) is still only an
uninvaginated optic vesicle and the lens is flat and useless.

or that they might have been derived from the photosensory ganglion
cells of Hesse's organs or the similar 'Joseph's cells' in the head region
of Amphioxus (Fig. 45, dc).

Studnicka's Theory — Unfortunately the cytogenesis of the rods and
cones supports neither Balfour nor Boveri, but confirms a radically dif-
ferent hypothesis first offered in 1912 by Studnicka, and which has yet
to be given consideration in any of the various text-books which afford
a little space to the eye-origin problem (Fig. 54) .

STUDNICKA'S THEORY

127

Studnicka noticed that if one traces the visual-cell side of the inner
layer of the optic cup around the latter and through the optic stalk into
the central nervous system, one emerges into the ependymal layer of the
brain wall. The ependymal cells lining the cavities of the brain and cord
are non-nervous supporting elements which often bear flagella (micro-
scopic whiplashes) which circulate the cerebrospinal fluid. Studnicka
also laid great stress upon the eye of the young larval lamprey (Fig. 54c) ,
which is precociously functional while still merely an optic vesicle, as
indicating that the vertebrate eye was originally merely a 'directional'

Fig. 55 — Comparability of young visual cells with ependymal and other flagellated cells:
embryological support for Studnicka's theory. From Walls.

a, fetal human foveal cone, showing filamentous, centrosomic anlage of outer segment rooted
in diplosome (after Seefelder). b, immature human sperm cell showing anlage of flag-
ellum, consisting of centrosomic filament and diplosome (after Gatenby and Beams), c,
immature cone from retina of kitten (after Leboucq). d, ependymal cell from brain of
carp (after Franz).

one before it became capable of forming images. Since the lens is already
present in the tiny lamprey, but in the form of a flat cushion incapable
of dioptric function, Studnicka argued that it must have existed phylo-
genetically — a vestigial remnant of something else, possibly a sense-
organ — before the retina was devised at all. He also showed that there
are many central-nervous sense-organs in vertebrates, including the
median or pineal and parietal eyes (see Chapter 10, section D), whose
receptors are certainly modified ependymal cells. He has received strik-
ing confirmation in the recent demonstrations of the photosensitivity of
the lining of the diencephalon of many forms, which (in birds) has been

128 THE GENESIS OF THE VERTEBRATE EYE

shown by Benoit and others to act as a photic receptor organ, controlling
reflexly the annual spermatogenetic cycle.

But Studnicka never considered in detail the manner in which rods
and cones differentiate, though this had already been most carefully
worked out by several European investigators. If he had done so, his
theory would surely have seemed much stronger to subsequent text-
writers. For the outer segment, the receptive organelle, of a vertebrate
visual cell develops exactly like any flagellum (Fig. 55a, b). It starts as
a filament of centrosomic material rooted in a diplosome or dumb-bell
shaped centriole embedded in the future inner segment, later becoming
encrusted and thickened by mitochondria which form the conspicuous
spiral filaments making up the bulk of the outer segment (Figs. 23a,
25c, pp. 55, 62; Fig. 26b, B, p. 63). A closer comparabiUty of visual cells
and ependymal cells (Fig. 55c, d) could hardly exist.

Origin of the Retina — If the photosensory parts of the rods and cones
were once ependymal flagella, it is certain that Boveri's theory must be
discarded; for ependyma, even photosensory ependyma, exists in Am-
phioxus side by side with the Hesse's organs and Joseph's cells. It is
equally certain that the vertebrate retina could not have gotten started,
as a photosensitive region of the brain wall, until the latter had become
tubular. Only then was there any need for the ependymal cells to evolve
as elements distinct from nerve cells; and these were primarily supportive
(they still run through the whole thickness of the brain wall in Am-
phioxus and the lampreys), then secretory in function (producing the
cerebrospinal fluid) before it became necessary for them to aid in circu-
lation by means of flagella. No flagella, no sensitivity or photosensitivity;
and it can be regarded as certain that the definitive visual cells were
developed within the finished brain and not, a la Balfour, while the nerv-
ous system was still a part of the skin. Indubitably there were photo-
irritable cells in the provertebrate's skin, as there still are in many fishes
and amphibians — even in cave forms which are never normally struck by
light; but these lost importance as soon as photosensory ependyma had
appeared (Fig. 56). The most primitive homologues of the rods and
cones to which we can point today are the photosensory flagellated epen-
dymal cells of the 'infundibular organ' of Amphioxus (Fig. 45, inf, p.
120), which is a crude visual apparatus seemingly for the detection of
the direction of light by means of shadows cast upon it by the anterior
pigment spot.

ORIGIN OF THE RETINA

129

Fig. 56 — Origin of the retinae of the median and lateral eyes. After Walls.

a, pro-vertebrate stage with photosensory ectoderm and with the nerve cord still a part of
the skin, b, b', alternative stages in the evolution of the neural tube, depending upon
whether one adheres to the 'solid' or 'hollow' doctrine, c, tubular nervous system formed,
but with ependymal lining purely sustentative, secretory, and circulatory, d, ependyma has
become photosensory locally, and photosensory cells have disappeared from the skin,
e, f, g, stages in the evolution of patches of photosensory ependyma into retinae.

Origin of the Lens — When everything else in the primitive eye is so
plausibly explicable, it is really a shame that we cannot be at all sure how
the lens came into existence. The lens placode fits neatly into the set of
cephalic lateral-line organs, and for it to develop into a lens is no more
remarkable than for one of them to generate the olfactory organ or for
another of them, the otic placode, to differentiate into the elaborate

130

THE GENESIS OF THE VERTEBRATE EYE

membranous labyrinth of the internal ear. It would be nice to be able
to insist that the lens placode has a real morphological existence and
that the lens is therefore a captured lateral-line organ, as Sharp be-
lieved; but we cannot do so with clear consciences. The best that can

i/m

Fig. 57 — Illustrating Tretjakoff's theory. From Walls, after TretjakofF.

a, foveolcB opticas stage, b, stage of closed neural tube, showing hypothetical chorioid
plexus, cp. c, hypothetical stage in which the expansion of the chorioid plexus has created
the pigment epithelium and, by forcing the sensory retina to curve, is producing a two-
layered cup. d, stage in which the attachment of the cup to the skin is evoking a muscle,
m, and a lens, /; a remnant of the chorioid plexus forms the umbraculum, urn, corresponding
to the pupillary nodule of an amphibian, e, final condition of fish eye with free lens, /,
operated by retractor lentis muscle, Im; from the umbracular remnant um a lens may be
regenerated, as in salamanders (cf. Fig 106a, pn, p. 266).

be said is that perhaps a former self-determination of the lens has been
replaced by a more convenient immediate chemical control by the optic
vesicle — just as the development of a secondary sexual character may
be under genetic control in one species of bird, while in another the

ORIGIN OF THE LENS 131

same character is caused to develop by hormones, and fails to appear
if the gland which secretes the chemical determinants is removed.

No other current explanation of the lens is anything but lame. The
co-existence of a functional retina and a functionless lens in the larval
lamprey may mean, as Studnicka thought, that the lens existed in some
other status before the rest of the present eye evolved. Possibly how-
ever it means no more than does the precocious presence of function-
less muscles in an embryo before their nerves have grown out to connect
with them. No one would argue that this means that those muscles once
functioned without nervous control.

/-/-^

Fig. 58 — Illustrating Schimkewitsch's theory. From Walls, after Schimkewitsch.

a, hypothetical ancestral skin-eye, with erect retina and intrinsic 'retinal' lens rl. b, phylo-
genetic stage comparable with embryonic cup — the eye, originally dorsal, has swung laterally
and ventrad, becoming passively indented (by resistant tissue) to create the embryonic
fissure; the retinal lens is now uselessly located, c, final condition of the eye, with new
lens derived from the skin; it is from the site of the supposed original retinal lens that
new lenses may be regenerated if the skin-lens is removed in the young embryo or even
(salamanders) in the adult.

Tretjakoff thought that the primitive optic cup was attached to the
skin and developed contractile elements there (which later became the
piscine retractor lentis muscle) for producing to-and-fro accommoda-
tory movements of the optic cup relative to the skin. The lens then
arose as a sort of callus in response to the continual pull of the muscle
cells (Fig. 57). But the lower fishes have no retractor lentis; and in any
case there would have been no need whatever of accommodation until
the lens had already appeared and become capable of forming a crisp
image. Tretjakoff also attempted to account for the fact that in sala-
manders whose lenses are removed, new lenses may regenerate from the
dorsal pupil margins. This has been explained more cleverly, if no more
properly, by Schimkewitsch (Fig. 58).

Franz's theory is new and ingenious. He suggests that the lens
evolved, when the neural tube was just closing, in such a position as

132

THE GENESIS OF THE VERTEBRATE EYE

to concentrate light upon the photosensitive lining of the diencephalon.
Its locus somehow escaped involution with the neural tube and later
moved laterally to be taken over by the new retina (Fig. 59) . No onto-
genetic conditions support this idea, and like the placode theory it stands
or falls with the demonstrability of a self-differentiating lens anlage.

Fig. 59 — Illustrating Franz's theory. From Walls, after Franz.

a, ancestral surface eye corresponding to the infundibular organ of Amphioxus prior to the
closure of the neural tube, b, later stage corresponding to the foveola; opticEe, with the
future lens-forming area labelled la. c, stage of general photosensitivity of lining of dien-
cephalon. The lens (shown in an earlier stage on the left, a later one on the right) is
evolving just outside the region of involution, d, stage of appearance of dorsal diencephalic
evagination — the future pineal eye; the lentogenic areas have shifted still farther laterally.
e, final condition of the pineal (p) and lateral eyes (/e); the lens is now embryologically
derived from the skin far distant from its original location.

The experimental morphologists are very fond indeed of doing things
to embryonic eyes to see what they will do in return. Someday, their
juggleries may disclose that in some species of fish or amphibian a lens
will start to develop without the presence of an optic vesicle. Until

ORIGIN OF THE LENS 133

then at least, and perhaps forever, the evolutionary origin of the verte-
brate lens must remain a tantalizing mystery.

A very good question is: how is it that the lens, derived from the
skin, lies inside the fibrous and uveal tunics— which, above, we homolo-
gjzed with the meningeal coats of the brain? Did the retina acquire its
optical partner before the central nervous system acquired its protective
sheaths? Perhaps so — and, such theories as that of Tretjakoff make such
an assumption necessary. But the lens could easily enough have gotten
through the sclerotic coat after the latter had evolved. Such legerdemain
is common enough in vertebrate history^as witness the presence of the
pectoral girdle inside the rib basket, in the turtles. All that is needed is
a nice timing of embryological events, occurring as an embryonic muta-
tion— if the lens did pass through the dura mater to get inside the eye-
ball, ii assuredly did so in one jump, in some ancient embryo in which
the condensation of the dura happened to be delayed. And lenses have
been getting inside of eyes ontogenetically in that same way ever since.

Chapter 6
ELEMENTS OF VERTEBRATE PHYLOGENY

If one knows something of the history of a group of animals and
its position in the animal kingdom, one may more easily draw correct
conclusions as to how it acquired its characteristic morphology. We
may learn of some structure in the eye of one of the lower animals which
looks intriguing as a possible forerunner of some detail of the human
eye; but we need to know whether the group that exhibits the structure
in question is anywhere near the main line of evolution, or represents
a blind alley from which nothing higher than itself has ever emerged.

A little about vertebrate group inter-relationships is therefore included
here, that the reader may better understand why one animal has solved
a given visual problem in one way while another, given other raw
materials, has had to find a different — perhaps better, perhaps poorer —
solution to the very same problem. In devising adaptive structures, each
animal group has had to do what it could with the materials at hand —
the assemblage of characteristics and structures with which the group
happened to be endowed when it crystallized out of the stream of life.
May we reasonably look to the teleost fish for the prototype of some
amphibian ocular structure? Can we expect to see in the snakes a feature
which the lizards discarded? Can we fairly compare the human eye more
closely with the eye of a salamander, or with that of a bird? A brief
review of the vertebrate pageant will help the reader to answer such
questions as they arise during his study of subsequent chapters.

At the bottom of the vertebrate scale stand the cyclostomes; and just
above them, the many types of true fishes. From one of these types the
first land animals, the ancient amphibians, were derived. They in turn
gave rise on the one hand to the modern amphibians and on the other
to the reptiles. The reptiles differentiated into a large number of orders,
only four of which have persisted to the present day. From one group
of extinct reptiles came the birds; and from another (much older) group,
the mammals — warm-bloodedness and heat-retaining coverings (feathers,
fur) thus having originated independently in the two highest classes of
vertebrates.

134

ELEMENTS OF VERTEBRATE PHYLOGENY 135

The lowest of the vertebrates are the cyclostomes, so named for their
round, suctorial, jawless mouths. The cyclostomes include the hags,
whose eyes are microscopic and functionless, and the lampreys (Fig. 60).
They are eel-shaped, blood-sucking parasites upon fishes. Some small

[Higher Placentals|
Insect I vores]

[Marsupials^

[Monotremes

t Therapsidans

t[Stegocephalians|!T|Coecilians[

iHolosteans', ' ' ^ |Cladistians[ /^; ^rossopterygiansj

>^ ^/" 'Dipnoansj

[Modern Chondrosteons^

Primitive
Chondrosteans

L^

.Selachians

Chinnaeras

I Primitive
Elasmobranchs

Primitive
Cyclostomesl

^Lampreys!
^Hagfishes]

Fig. 60 — Inter-relations of the major groups of vertebrates.
Only those extinct groups (marked f) are shown which actually link up living assemblages.

freshwater lampreys have given up parasitism and do all of their feeding
as larvae, breeding for the first and only time a few months after trans-
forming to the adult condition. Parasitic lampreys also breed but once
after years of vegetative activity, and then die. Cyclostomes have no
scales or paired fins, and many other things about their anatomy are

136 ELEMENTS OF VERTEBRATE PHYLOGENY

simple; but it is sometimes difficult to know whether to attribute the
simplicities to primitiveness or to the secondary simplification (mistak-
enly called degeneracy) which is a part of their adaptation to a parasitic
mode of life. As regards the lamprey eye, however, there is unanimous
agreement among modern students that its features are all primitive
and show no indications of degeneracy.

The oldest of the true fishes are the elasmobranchs, whose modern
representatives, the Selachii (sharks and rays) and Holocephali (chim-
aeras), are very different from their extinct progenitors. The elasmo-
branchs were derived from ancient cyclostomes, but not from lamprey-
like ones. Like the cyclostomes, they have cartilaginous skeletons; but
they also have paired fins, jaws, and scales. From those jaws have come
the little bones of the ossicular chain which traverses our middle-ear
cavity; and from some of the rows of scales on the elasmobranchs' lips
came their teeth, the ancestors of our own — and very different from the
horny teeth of lampreys.

The primitive elasmobranchs were a main-line group, for from them
have come all of the higher, 'teleostome' fishes; and through these, the
terrestrial vertebrates. From ancient elasmobranchs there arose an ad-
vanced group of fishes, still with cartilaginous skeletons, called the
Chondrostei. These fishes have had many descendant groups, among
them several which might, any one of them, have given rise to land
forms — for they all spread into fresh waters and swamps, and developed
lungs of sorts, and limb-like fins with which to drag their bodies over
the slime.

These lunged fishes were the Cladistia, the Crossopterygii, and an
offshoot of the latter called the Dipneusti — the lung-fishes proper. All
three of these groups were once numerous as to species and individuals,
but have dwindled to remnants which still cling precariously to life in
competition with the more advanced modern fishes. The Dipneusti, or
dipnoans, have but three living genera : Neoceratodus in Australia (Fig.
61a), the African Protopterus, and Lepidosiren in South America.
There are but two living cladistian genera — Polypterus and Calamoich-
thys, both in Africa. Until very recently it was supposed that the cros-
sopterygians were extinct; but one species, named Latimeria chalumnce,
was lately discovered in the sea off South Africa. This is the only archaic
teleostome known from salt water.

The chondrosteans have persisted to the present time, but are now
represented only by the sturgeons (Acipenser, Huso, Scaphirbyncbus,

ELEMENTS OF VERTEBRATE PHYLOGENY 137

etc.) and the spoonbills or paddlefishes, Polyodon and Psephurus. Very
soon after their own origin, the chondrosteans gave rise to a group of
fishes with bony skeletons, the Holostei — formerly lumped with the
Chondrostei in an artificial group called the 'ganoids'. The Holostei had
their heyday long ago, and have but two living genera, the bowfin
(Amia) and the gars or gar-pikes, Lepisosteus spp. From primitive
holosteans came the Teleostei, the most conspicuous group of modem
fishes, including such familiar forms as the trout, perch, herring, and
goldfish. Defeating the holosteans in competition for habitats and food,
the teleosts have taken the place in the seas and fresh waters formerly
occupied in succession by the chondrosteans and holosteans. But the
teleosts are a blind-alley group from which no higher forms have been
derived.

Fig. 61 — The transition from water to land.

a, an existing dipnoan, the Australian 'dyelleh', Neoceratodus forstert. After Ley.

b, a giant stegocephalian, Mastodonsaurus giganteus (redrawn by E. C. Case, from a
restoration by Fraas); in life, the animal was about fifteen feet long, p- site of pineal eye.

It was probably from swamp-dwelling crossopterygians that the first
land vertebrates came. These were the extinct amphibians which we call
the Stegocephali, from their characteristic head-armor. Some adult stego-
cephalians were but a couple of inches long, but most of them were gross,
sluggish beasts of little brain (Fig. 61b) — very different from the pert
little salamanders and agile frogs of the present time. It is possible that
the Stegocephali are not a natural group, but comprise two groups with
independent origins. It is also barely possible that some of the modern
amphibians originated directly from air-breathing fishes and not from
the Stegocephali. These questions have only recently been raised and
are not yet settled. At any rate, it is certain that the Stegocephali were

138 ELEMENTS OF VERTEBRATE PHYLOGENY

the immediate ancestors of the reptiles — which, with their dry, scaly
skins and a number of internal improvements, were the first vertebrates
to become quite divorced from the waters.

The first land vertebrates must have had an easy time of it. Escaping
the fierce competition of the waters, they found themselves exploring a
new world in which they had no enemies. There was abundance of food,
for the plants had taken to the land eons before. The very ease with which
the land animals could spread and multiply encouraged the rapid pro-
duction of new types. And then, the inevitable happened — some of these
newer forms found the older ones good to eat. Competition on land
eventually became so keen that many reptiles, mammals, and even birds
returned to an aquatic existence. On land, their muscles had had to
sustain their weight and had become far more powerful than those of
fishes. Claws, beaks, and crushing teeth had also evolved, and with such
superior weapons many species found it easy to get a living in the water.

The reptilian group flourished amazingly and ruled the world for tens
of millions of years through its aristocracy, the group we call the dino-
saurs. But even while the twenty-foot tyrannosauri were mangling the
ninety-foot diplodoci, the first of the mammals were furtively sneaking
about looking for dinosaur eggs to suck, and the first birds — derived
from tiny dinosaurs — were getting off the ground for short flights. The
reptiles which we have around us are a mixture of old and new. The
lizard-like Sphenodon (rapidly approaching extinction on a couple of
New Zealand islands) is the sole survivor of the rhynchocephalians, the
rest of which died with the dinosaurs. The turtles are of enormous
antiquity — turtles are among the oldest reptilian fossils we know of,
and they were already perfectly standard turtles "way back then'. The
ancestors of the crocodile group can also be traced back into the begin-
nings of the Age of Reptiles.

The lizards, however, came into existence only recently as an offshoot
of the extinct mosasaurs. The snakes originated as legless lizards, so
very recently (as geological time intervals go) that the most primitive
of them, the boas and pythons, still have vestiges of the hind legs. Leg-
lessness has since arisen independently several times in different families
of existing lizards, but these snake-like forms are still true lizards.

The mammals fall into three great divisions: the egg-laying mono-
tremes of which only the duck-billed platypus (Ornithorhynchus) and
the echidnas are left on earth; the marsupials, which originated in South
America and left primitive types there, but reached their culmination

ELEMENTS OF VERTEBRATE PHYLOGENY 139

in Australia where they had no competition from the higher mammals;
and the placentals, which are the familiar hairy, milk-secreting animals
of the world and the group to which man himself belongs.

As one would expect, the birds, the monotremes, and even the mar-
supials have quite a bit in common anatomically with the reptiles. But
the placental mammals are quite distinct — more different from the mono-
tremes than the latter are from the reptiles. This is especially true as
regards the eye; and from ocular and other considerations Franz has
postulated that the placental mammals originated, not from lower mam-
mals, or (Huxley's view) independently from reptiles, but from forms
intermediate between the amphibians and the reptiles. There is however
no palxontological justification for such a view. The reptiles and birds
are so closely related that they are commonly lumped together as the
'Sauropsida'; and monotreme eyes — to some extent also marsupial eyes
— are sauropsidan in plan except for a radical simplification of the
mechanism of accommodation. The eye of the placental mammal is more
like that of an amphibian than like that of a reptile, but this is no proof
that the placental mammals originated more or less directly from am-
phibians. A more likely view is that the placental mammals had an early
history of strict nocturnality, during which they depended largely upon
other senses and simplified the eye far below the level of complexity of
the eye of the reptilian ancestor. The placental eye thus came to simulate
the amphibian eye through what might be described as a reversal of
evolution.

For our purposes the placental mammals may be roughly divided into
'lower' and 'higher' orders — the former including the insectivores, pri-
mates (including man), bats, sloths, armadillos, ant-eaters, and the 'fly-
ing lemurs' (Galeopithecus and Galeopterus) ; and the latter comprising
the carnivores, seals, whales, and hoofed animals (including the elephants,
hippos, etc.). The rodents and lagomorphs may be assigned to the top
of the lower series or to the bottom of the higher, depending on one's
point of view.

The tree-shrew and the aye-aye are thus at the bottom of the group
and the elk and tiger are at the top — with man very close to the bottom
biologically, ranking high only psychologically, as regards his brain and
mind. Man's order, the Primates, split away from the Insectivora about
50,000,000 years ago. Most of the living groups of mammals have come
into existence since that time. Man himself came along only yesterday,
but his stock is older than most of the mammalian stocks around him.

Part II-Ecologic

Chapter 7

ADAPTATIONS TO ARHYTHMIC ACTIVITY

(A) The Twenty-Four-Hour Habit and the Eye

Of the ways in which natural light can vary, it is the variation of
its intensity which is of most importance to animals, and to which they
have responded by the most profound of ocular modifications. To adopt
the bright hours of day, or the dim ones of night, or to appear indifferent
to their alternations, all require adaptations of the eye. These adapta-
tions for high sensitivity or for relative insensitivity in turn make pos-
sible, or tend to forbid, concomitant adaptations for form-perception
and visual recognition on a basis of pattern and color. Animals have
had to balance the desirability of a given habit with their ability to use
the advantages, and tolerate the disadvantages, which the modifiability
of their eyes in the appropriate direction confers or limits. In this and
the two succeeding chapters we shall examine the adaptations to illumin-
ation-preferences which vertebrate eyes have produced.

In surveying the visual habits of vertebrates one's attention is natur-
ally caught by the extreme conditions of strict diurnality and strict
nocturnality, and one tends to suppose that the intermediate condition
or arhythmicity, of apparent indifference to night and day, represents a
failure to specialize and a lack of adaptation. This is never actually the
case — a truly unspecialized and intermediate type of eye would fit its
possessor, not for twenty-four-hour vision, but for only the brief periods
of morning and evening twilight. The arhythmic animal has to meet a
more severe set of requirements than does the rhythmic one of either
extreme type, and meets them by combining in one visual organ those
adaptations to both bright and dim light which are not mutually exclu-
sive. To anticipate the next two chapters, a strongly yellow lens (as in
the prairie-dog) goes with diurnality but makes vision in dim light im-
possible; and a tapetum lucidum facilitates nocturnality but if non-

lusible and associated with a super-sensitive retina unprotected by a
lit pupil (as in the opossum) , it demands that the animal scrupulously
avoid strong light. Obviously, any attempt by an animal to secure twenty-
four-hour vision by combining a yellow lens with a tapetum would result
in his having wretched vision at any and all times.

143

occ

s

144 ADAPTATIONS TO ARHYTHMIC ACTIVITY

In either type of rhythmic animal we may have fancy adaptations, yet
an ocular situation which is simple in that it is static. But, for an animal
to become capable of arhythmic, twenty-four-hour activity, it is incum-
bent upon him to evolve a more flexible set of ocular features, capable
of physiological change to embrace a wide range of stimuli — in other
words, a dynamic eye in which, when the animal passes from one ex-
treme of illumination into the other, something or several things can be
seen to happen, and can be seen to be adjustive. The photomechanical
changes of the iris and the retina are the most conspicuous 'somethings'
referred to. Adaptation to twenty-four-hour vision has its static end-
products as well, in the evolutionary alteration of the cone: rod ratios
of a rhythmic ancestor, or even in the production of a duplex retina
from an ancestrally simplex one by the transmutation of cones into rods
or vice versa.

Before we take up these physiological and phylogenetic methods of
adaptation toward all-round visual capacity, it will be well to have
certain ecological definitions well in hand. We find that animals may
be classified as:

A. Diurnal; by which we shall take to mean that they are active
chiefly in the daytime, occasionally also in bright moonlight. Such
animals have eyes which are incapable of dim-light vision.

B. Crepuscular ; that is, active only in either or both of the evening
and morning twilight periods. Requires more sensitive eyes, which are
truly neutral, with few or no adaptations for extremes of illumination.

C. Twenty-jour-hour — more properly, 'arhythmic', the former term
applying better to both eye and animal, and both terms signifying that
the animal is about equally active by night and day. Such animals, if
they sleep at all, do so by irregular cat-naps.

D. Nocturnal; being active chiefly at night and confining daytime
activities largely to passive basking. Eyes usually more sensitive than
those of twenty-four-hour animals, and with much better devices for
greatly reducing sensitivity in daylight,

E. Strictly Nocturnal; with such sensitive eyes, so lacking in sensi-
tivity-reducing devices, that the animal is secretive or quiescent by day.

Each of these categories blends and intergrades with the next. Par-
ticularly is this true between 'C and 'D\ in which groups fall nearly all
of the mammals with the larger ones leaning toward 'C and the smaller
species inclining strongly toward 'D' or 'E'. The chief assemblages of

THE TWENTY-FOUR-HOUR HABIT 145

class 'C, twenty-four-hour vertebrates, and their principal bases for all-
round visual capacity, are:

The teleost fishes, relatively few of which are strictly diurnal, noc-
turnal, or crepuscular. Their ability to regulate ocular sensitivity resides
aknost wholly in their rod-rich retinae, in the form of efficient photo-
mechanical changes. Very few have mobile pupils.

The frogs, which again rely chiefly upon retinal adjustments and
possess at least one diurnal adaptation (yellow oil-droplets) which the
toads and the salamanders have had to eliminate, in order to become
respectively nocturnal and secretive.

Many slit-pupilled reptiles, which, being poikilothermous, tend to
bask in the sunshine rather more than would a warm-blooded animal
with the same general type of eye. The crocodiles and particularly the
geckoes have such excellent pupillary control of sensitivity that they
are practically arhythmic though tending to feed more at night.

The larger terrestrial mammals — ungulates, elephants, and large car-
nivores such as the wolves, bears, lion, etc. Here alone do we find
twenty-four-hour eyes which physiologically are relatively static, with
neither special retinal nor, as a rule, extensive pupillary regulation of
sensitivity. These forms straddle the fence by having enough rods-per-
cone to secure fair intrinsic retinal sensitivity, with large eyes and large
retinal images to obtain good resolution of details despite the paucity
of cones. They compensate for the lowered illumination of the larger
image by placing behind the retina a sensitizing device, the tapetum,
which is elsewhere found chiefly among the best-adapted of nocturnal
vertebrates. The vision of these mammals both by night and by day is
good enough so that they depend on it. Hearing and scent are important
enough at long range, but the serious business of stalking involves vision,
whatever the illumination. Day or night, a sightless carnivore would be
helpless — and so would a blinded ungulate.

(B) Retinal Photomechanical Changes

The phenomena which are grouped under this heading were discovered
one by one in the 1877-1887 decade. They consist of changes of position,
in bright and dim light or darkness, of the retinal pigment and the visual
cells, and of minor changes in shape and position of some of the retinal
nuclei. The nuclear changes are largely passive and are of no known
significance for vision; but the migrations of the rods, cones, and retinal
pigment are of great importance in the lower vertebrates.

146

ADAPTATIONS TO A RHYTHMIC ACTIVITY

Pigment Migration — It will be recalled that the cells of the retinal
pigment epithelium often bear groups of long processes which interdigi-
tate with the visual cells (Fig. 20d and e, p. 44) and that in the latter
a portion of the inner segment between nucleus and ellipsoid is often
contractile and then bears the name of myoid (Figs. 22, 23, 24; pp. 54,
55, 59). It is the retinal pigment (fuscin) in the pigment-cell processes,
and the rod and cone myoids which are chiefly concerned in the photo-
mechanical changes of the retina. These changes are most conspicuous
in duplex retinae and are concerned with both light- and dark-adaptation
of the retina.

Fig. 62 — Photomechanical changes in the retina of a fish, Phoxinus lavis.
From Kiihn, after von Frisch.

a, visual-cell layer and pigment epithelium in light-adaptation, b, dark-adaptation.
e- pigment epithelium; r- rods; c- cones; /- limitans; n- nuclei of visual cells.

When an animal equipped with photomechanical changes emerges
into bright light, a large portion of the retinal pigment — that which is
in the form of rodlets or short needles rather than tiny spherules — starts
to flow slowly down into the pigment-cell processes. These may be num-
erous and so slender that the granules pass into them in single file, or
they may be fewer and much more bulky. In as little time as half an hour
(though usually more slowly) the pigment will be found to be largely
scattered along the length of the processes and may reach nearly to the
external limiting membrane, being piled up into a dense mass at this
limit of its excursion. It thus forms a system of cylindrical sheaths sur-

RETINAL PHOTOMECHANICAL CHANGES 147

rounding the visual cells and blocking off from them any light rays
which approach them at angles to their axes. Where the myoids are very
slender (as in most fish rods) the expanded pigment may close in densely
enough between the rod ellipsoids and the limitans to shut off even the
axial rays from the percipient outer segments of the rods (Fig. 62) .

Fig. 63 — Visual-cell migrations in a catfish, Ameiurus nebulosus. x 500.
After Welsh and Osborn.

a, depigmented section of light-adapted retina, showing rods elongated toward pigment
epithelium and cones retrarted toward external limiting membrane.

b, depigmented section of dark-adapted retina; cones elongated, rods retrarted.

Visual-Cell Movements — Cones always escape being thus shielded to
any extent by the expanded, light-adapted pigment. They either sit,
permanently, directly upon the limitans or, if migratory, contract into
that position — away from the advancing pigment — in the light. Rods how-
ever, if they migrate at all in bright light, do so in the direction toward
the pigment (Figs. 62 and 63), The effective covering of the rods by
pigment is thus the sum of the pigment expansion and the elongation of

148

ADAPTATIONS TO ARHYTHMIC ACTIVITY

the rod myoid. The two movements are not perfectly synchronized, how-
ever, for the visual cells usually complete their migrations much more
rapidly than does the retinal pigment, though always consuming from
several minutes to an hour or more in the process, in different species.
There may be both indefinite and very definite differences within a single

Fig. 64 — Photomechanical changes of the leopard frog, Rana pipiens. x 500.

a, ventral periphery of light-adapted retina. The expanded pigment obscures the visual cells,
but a cone and a rod have been emphasized to show their positions.

b, same region, dark-adapted. The outlines of the visual cells have been reinforced. Note
that the cone myoids are greatly lengthened, the rod myoids somewhat shortened, as com-
pared with a. Toward the right is a double cone, whose chief member has migrated but
whose accessory member never leaves the limitans (c/. Figs. 22c, 23d, 24b, pp. 54-59).

retina, for the cones may be either uniform or very ragged in their re-
sponses, and both pigment and cones may respond less in particular
retinal areas than in others. In fishes the single and twin cones migrate
at different rates to different extents, and in other vertebrates the acces-
sory members of double cones never migrate whether the chief cones do
or not (see Fig. 24, p. 59, and Fig. 64b) .

SIGNIFICANCE AND DISTRIBUTION 149

If the animal now enters darkness or even a dimly-lighted situation,
the movements proceed, more slowly than in light-adaptation, to reverse
themselves : the pigment granules glide back up out of the processes and
concentrate as a dense band in the cuboidal cell-bodies of the epithelium,
the rod myoids shorten and draw the sensitive outer segments away from
the pigment and thus toward the light, and the cone myoids elongate to
push the cone bodies toward the pigment — sometimes to no apparent
purpose, but in some animals thereby making appreciably more room for
the rods to gather in a smooth layer close to the limitans (Figs. 62, 63,
and 64).

Significance and Distribution — Where the photomechanical changes
are as complete as described above, and carried out smoothly and within
an hour's time or less, the whole machinery is clearly of great value in
adjusting the retina to the external illumination. The workings of the
Duplicity Theory are beautifully seen in these phenomena, for the cones
are most advantageously placed for action in bright light, the rods being
then shielded from excessive stimulation (or from any at all) ; and in
dim light the rods are fully exposed while the cones get out of their way,
whether this latter happening has any obvious value or not. As a device
for equalizing the actual stimulation permitted to the visual cells in
various illuminations, the photomechanical system at its best is excellent
and has only the single drawback of slowness. Even this defect may be
unimportant in the case of an animal with sedentary habits and deliber-
ate movements, for temporal changes in natural illuminations are rarely
rapid. But the low speed of the retinal migrations would seem to be
detrimental to an agile species which flits from light to shade sporadic-
ally and lacks any more rapid means of regulating the illumination of
its visual cells. Among such forms would be fishes which move rapidly
from the bright surface to the dim depths and vice versa, and those
which inhabit coral reefs and the like, which may help to explain why
the latter are commonly crepuscular.

Table II summarizes the occurrence and relative effectiveness of the
photomechanical changes in the various vertebrate groups. The reader
will note a general tendency for them to dwindle in importance as one
passes from lower to higher forms, the reason for which will be discussed
in Section C.

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150

IMMEDIATE CAUSATION 151

Immediate Causation — It is evident from the table that there are few
important vertebrate types about whose photomechanical changes, or
lack of them, we cannot make positive statements in a descriptive way;
and the reader has just been promised an integration of the apparent
hodge-podge of their distribution, and an interpretation of the phylo-
genetic degeneration of these ingenious phenomena. But there is no
branch of physiology which is in a less satisfactory state than the whole
matter of the immediate nature, causation, and control of the photo-
mechanical changes.

The unwieldy literature of the subject is full of contradictory con-
clusions based on seemingly equally sound lines of evidence, on failures
to take account of the great individual physiological variability of the
lower vertebrates (particularly the amphibians!), and on simple ignor-
ance of other workers' results, especially of conclusive negations of some
of the pioneering researches.

We do not even know whether either extreme position of the retinal
pigment or of the rod or cone myoids represents a condition of relax-
ation, or whether the expansion and retraction of the pigment and the
elongation and shortening of myoids are all active processes. We can
glibly say that the movements of the pigment are "due to protoplasmic
streaming" but (though it could easily be ascertained on isolated epi-
thelium in vitro) we do not know whether the pigment cell can respond
in either direction, autonomously and directly, to light and darkness.
We have no conception whatever of the intracellular mechanism which
changes the length of a myoid, though these changes are enormously
greater than those which take place in a striated muscle cell whose
fibrillar machinery is fully revealed to microscopic view. And we are
greatly puzzled by the fact that apparently the same stimulus, or lack
of stimulus, which causes the myoid of one visual-cell type to elongate,
simultaneously causes the other to shorten. It is known that myoid vol-
umes remain constant at all lengths, and that shape-changes elsewhere
in the visual cells are purely passive. It is known that contractile cone
myoids respond by shortening in the presence of acids, and that retinae
which contain cones are acid in the light and alkaline in the dark.
Studnitz has injected phosphoric acid into dark-adapted fishes and found
that the pigment and cones took their 'light' positions. Injections of
alkali into light-adapted fishes made them dark-adapt. Studnitz thinks
that even the effects of adrenalin chloride are due to its acidity, not to
the hormonal base. To what it is that rod myoids respond, and how, no

152 ADAPTATIONS TO ARHYTHMIC ACTIVITY

one can say. Contractile ones look no different from non-contractile;
and there are such paradoxical situations as that in the frog, where the
common 'red' rods, with stubby myoids, have a respectable migration
while the scanty 'green' rods, with very long myoids like a teleost rod
or a dark-adapted frog cone, move but little if at all (see Fig. 23, p. 55).

The photomechanical phenomena are interesting enough and baffling
enough in their normal operation, but perhaps the most remarkable thing
about them is that they may actually work better when out of their
normal environment : it has been found that the pigment and cone move-
ments become almost twice as extensive in a salamander eye which has
been transplanted, in the larva, into the location of the ear!

As to the control of the movements, opinion is divided between two
schools of thought. Most of the work — not all — on fish material indi-
cates that efferent nerve impulses control the movements. Cutting one
nerve to the eye may halt the migrations, and cutting another in addition
may let them recommence. In one fish, the day-night rhythm of the retina
is known to persist even in constant darkness; nor does a frog stay dark-
adapted in darkness — in a few hours the cones elongate, then shorten.

Much of the reported work on amphibian material favors the idea of
control by blood-borne substances. Nerve-cutting has little effect, vessel-
ligation a considerable one. The transplanted eyes referred to above were
entirely divorced from nervous control, but adequately vascularized. The
effects of drugs, narcotics, and anaesthetics are ambiguous. The effects
of temperature are especially mysterious, for both high and low tempera-
tures cause light-adaptation in the dark and inhibit the dark-adaptation
of previously light-adapted animals. Excised dark-adapted eyes will light-
adapt readily, but excised light-adapted eyes will dark-adapt only in the
surprisingly special environment of a second frog's body cavity. Emo-
tional states interfere with the phenomena, but these could have their
effects by means of either nerve-impulses or hormones. Yellow light is
more effective than other colors, speaking either for a reflex control from
the visual apparatus itself (as in the case of iris reactions in higher ani-
mals) , or for a direct influence of acid, formed maximally in the retina
under yellow light. On the other hand, old evidence — still commonly
cited — for reflex effects from one eye to the other and from the skin to
the eyes is under grave suspicion, for in the experiments the animal's
breathing was interfered with and fear was introduced, by the employ-
ment of leather hoods. Either of these factors is now known to be
enough to make a frog light-adapt, though he be in darkness.

FUNCTIONS OF THE PUPIL 153

The whole subject requires a very careful review and deserves the
attention of at least one cautious investigator prepared to devote his
active career to it. Practically everything which has been done in the
way of experiments upon the mechanism of the phenomena needs re-
peating with better technique than has been used. Not a single experi-
ment has yet been made with all factors controlled, nor a single graph
plotted with nearly enough animals averaged at each point. The photo-
mechanical changes are so fascinating that their students have been a
little too impatient to know what makes them go.

(C) Pupil Mobility

Functions of the Pupil — The pupil ordinarily has two chief respon-
sibilities. It must fix the immediate illumination of the retina, if it can,
at a value above the threshold of stimulation and below the point of
dazzlement or injury; and it must restrict the perceived light-pencil to
the center of the lens as far as possible. The pupil may be relieved of one
or the other of these duties. Thus in the chameleons the lids are fused
to the surface of the eyeball and their opening is a small one which
'stops down' the broad lens without benefit of changes in pupil diameter.
Again, a strongly nocturnal animal may so conduct himself that he is
seldom or never exposed to bright light, and his wide pupil may not
need, or have, much ability to close down, to convert a dazzling external
illumination into a tolerable intra-ocular one.

Though not at all exceptional, such conditions are nevertheless assoc-
iated with the extremes of diurnal and nocturnal adaptation and be-
havior. The pupil may have little to do in a night-prowling species which
conceals itself well in the daytime and has no wish to bask in exposed
positions. It may have little to do in a sun-worshipper whose pure-cone
retina is so insensitive that various natural brightnesses above his thresh-
old are about equally comfortable to him. The slit pupils, so characteristic
of those nocturnal forms which do court the sunshine, deserve special con-
sideration beyond the scope of this discussion (see Chapter 9, section C) .

The need for considerable pupil 'excursion' — range of size change —
is thus the greater, the more the animal attempts to attain twenty-four-
hour visual capacity. In such animals the responsibility of the pupil and
its controlling mechanism is greatest also, for the two aims of the pupil
are increasingly at cross-purposes when the period of daily activity be-
comes longer and longer. In the brighter hours, the closure of the pupil

154 ADAPTATIONS TO ARHYTHMIC ACTIVITY

serves both of the aperture's functions equally well; but as the animal
attempts to make use of the evening and night hours, or to set back the
alarm-clock in the morning, the pupil must walk an increasingly precar-
ious tight-rope. It must open far enough to permit of stimulation, but
not so far that the blurring of the image takes more away from vision
than the increased light confers. Fortunately, as the intensity falls very
low, the widening pupil finally begins to add more to the quality of the
image, in brightness, than it takes away, by aberration. As day passes
into night, the now familiar acuity-sensitivity seesaw (p. 69) begins
inexorably to move. In any but a very strictly diurnal animal, sensitivity
goes up, perhaps very high; and in any and all animals, acuity inevitably
comes down.

A highly mobile, precisely controlled pupil prepares its owner for both
night and day. We have seen that the same can be said for a well-devel-
oped system of photomechanical changes. An active iris in a given animal
may be free to give its whole allegiance to illumination, or its movements
may be tied reflexly more closely to accommodation, convergence of the
two eyes, or emotional changes, or may even be under the control of
the will. The pupil may be so blocked by the lens that its closure is
impossible unless the iridic sphincter is able actually to compress the lens
(a possibility which, as an adaptation to amphibious habits, is realized
in some vertebrates) . In the majority of fishes, the blockage is so com-
plete and the lens so firm or so large that any attempt at pupil movement
is hopeless and the iris is actually devoid of muscle.
Pupillary versus Retinal Adaptation — Being more familiar with
movable pupils, we are likely to think of the photomechanical changes
in the retina as being able to save such situations, and take the place of
extensive pupil mobility. Historically, it has really been the other way
'round; for as we saw in the preceding section, the phylogenetic history
of the photomechanical changes has been one of fairly steady reduction
from a peak in the teleosts to complete absence in the mammals, the
birds being exceptional, since in them, despite their high position and
their mobile pupils, the photomechanical changes have been resuscitated
for special reasons which will later be set forth.

Concomitantly, there has been a steady development of pupil mobil-
ity— among twenty-four-hour and nocturnal animals — from nothing in
most fishes to a maximum in the mammals. We may reasonably expect
to find then, at any evolutionary level, one or the other of these regula-
tory mechanisms in good condition (consult Table II, p. 150).

PUPILLARY VS. RETINAL ADAPTATION 155

A pure-rod animal may need neither photomechanical changes nor a
mobile pupil, if he is content to be strictly nocturnal; and a diurnal ani-
mal will need neither very badly if he has a pure-cone retina and can
afford to be blind in dim light and utterly dependent then upon other
senses — as a pure-cone retina necessitates. But if a form whose retina is
duplex is to be able to appear indifferent to depth of water or to night
and day, or if a pure-rod animal is to be able to bask in comfort and to
defend itself from an enemy which routs it out of its daytime slumber, it
must have a widely excursive pupil or effective photomechanical changes.
Only one other mechanism, of limited value and with primarily other
functions, can sometimes be called into play for the regulation of stim-
ulation : the lid apparatus — sometimes, as regards its awning-effect, sub-
stituted for by projections on the upper part of the iris. The importance
of the lids in this connection can best be judged from instances in which
they are absent. Thus for example in the rays, the vipers, and the geckoes,
movable lids are lacking and the pupil is capable of an exceptional degree
of closure as compared with relatives which do have functional lids.

We can expect to find that a pupil will tend to open unless something
makes it close. The inherent elasticity of the connective-tissue stroma of
the iris tends to insure this, and in some animals, notably certain small
mammals in which a dilatator is lacking, it is the only antagonist of the
sphincter. Where there is a dilatator, it is a thin sheet, but a broad one ;
and its total bulk compares favorably with that of the sphincter. One or
the other may be the stronger in a given case; but the orientation of the
dilatator, other things being equal, gives it a big advantage over the
sphincter. It is as though the two muscles are pulling on opposite ends of
a lever of the first class, the ratio of whose arms is 3.1416:1; for the
sphincter, contracting around the periphery of a circle, must shorten
TT units while the radially-oriented dilatator relaxes one unit, and the
sphincter cells must be capable of contracting TT times as fast. Of course
if a pupil can move at all it can both open and close; but it is sometimes
more important for it to open in dim light than for it to close in bright.
Where the pupil is static, it is even more necessary for a nocturnal an-
imal to have a large one than for a diurnal animal to have a very small
one, for the latter can always partly close his lids. Where it is mobile,
it is more desirable for a nocturnal pupil to close promptly in bright
light than for it to open so suddenly in dim light, where the accumu-
lation of rhodopsin is very slow anyway. Hence it is that many a small
nocturnal animal has a powerful sphincter muscle and no dilatator at all.

156 ADAPTATIONS TO ARHYTHMIC ACTIVITY

In emergency situations, in the higher vertebrates, the pupil seems to
try to make sure of enough light — its response to pain, to rapid deep
breathing, or to strong emotion of any kind is to dilate, sometimes so fast
and far (as in the hyaenas) as to seem to be under the animal's control.
Close scrutiny of an object, ordinarily a calm and non-emergency proce-
dure, is on the other hand accompanied by contraction. This 'accommo-
dation reflex' is not a true reflex, but a fortunate accident of innervation.
The iris sphincter and the ciliary muscle are supplied by the same nerves.
The 'reflex', which in man occurs more with convergence than with the
accompanying accommodation, and is in that aspect truly reflex, is of
some value in all its possessors (though of most value in those vertebrates
whose irides actually aid in accommodation; see Chapter 11, section C).
In its accommodated form the lens has more spherical aberration. It
therefore needs more stopping-down, and receives this upon the reflex
closure of the pupil, thus increasing resolving power for approaching ob-
jects. As objects approach, the amount of light received from them in-
creases enough to compensate adequately for any accommodatory reduc-
tion of the area of the pupil.* Another pupil reflex in man, of no obvious
value, has recently been described : it consists of a slight contraction at
the moment of fusion of the two monocular images into a single stereo-
scopic one, as when one is observing through a stereoscope.

In the birds, whose photomechanical changes are more conspicuous
than one would expect from the phylogeny of the changes and of the
pupil, the reason appears to be that the bird pupil pays less attention to
illumination than to accommodation and emotion. The 'play' of the
pupil of a captive wild bird will readily convince one of this, though the
irides of tame birds, such as chickens, may react quite staidly to light.
There is thus no inconsistency in the fact that the birds have both iridic
and retinal photomechanical changes well developed (Table II, p. 150).

The behavior of the pupil is influenced more immediately, as well as in
in the long evolutionary run, by the presence or absence of retinal migra-
tions. The first reaction of a pupil (i.e., partial closure) upon a sudden
increase of illumination is not permanent. It gives opportunity for the
retina to reduce its sensitivity; and when this has been sufficiently effected,
the pupil slowly reopens to a size which is smaller than its original one,
and is constant until a further great change in intensity. This physiolog-

*In the dog, according to Nicolas, the accommodation reflex works backwards — the pupil
dilating for near, contracting for distant objeas; and there is no consensual reflex. These
peculiarities have yet to be explained.

PUPILLARY VS. RETINAL ADAPTATION 157

ical adaptation of the pupil is to be sharply distinguished from the imme-
diate reaction it gives to increased illumination. Upon a reduction of
illumination the pupil only dilates to a new constant size, there being
rarely a brief preliminary contraction. The rate of the complex light-
adaptation and of the simpler dark-adaptation of the pupil depends upon
the method by which the retina changes its sensitivity. When only cones
are present, as for example in diurnal snakes, the change in sensitivity is
slight and rapid and the pupil also makes quickly the slight adjustment of
which it is capable. Where many rods (but no photomechanical changes)
are present, as in the guinea-pig for instance, the light-adaptation of the
pupil is governed by the relatively rapid destruction of rhodopsin. Where
both rods and photomechanical changes are conspicuous the rhodopsin is
more abundant and, especially in fishes and owls, slow to bleach. The
pupil then adapts much more slowly (frogs) or not at all (fishes) , since
retinal sensitivity is altered primarily by the relatively slow pigment
migration. It is in fact quite probable that in the teleosts the rhodopsin is
seldom all bleached, since the rods are completely shielded by expanded
pigment. Higher vertebrates, it would seem, must be able to form more
rhodopsin since so much must be destroyed at every light-adaptation.
Very likely, the greater instability to light of the rhodopsins of higher
vertebrates (through which the rhodopsin is quickly destroyed, and the
threshold of the retina as quickly raised) is partly a consequence of the
lack of such perfectly protective photomechanical changes as the lower
vertebrates possess.

Pupil movements are thus not only less marked, but less rapid, in prim-
itive forms which still depend primarily upon retinal migrations. Phyloge-
netically there has been a steady perfection not only of the pupil as an
adjusting mechanism, but also of its method of actuation and control. In
the few fishes which have iris muscles, these are pigmented and respond
directly and autonomously to light — the sphincter by contracting, the
dilatator by losing tonus. These actions are extraordinarily slow — elas-
mobranch pupils take two or three minutes to close in bright light and
an hour or so to re-open in the dark! Such muscles are unresponsive to
electrical stimulation and to neurotropic drugs like atropin, since such
agencies operate through nervous connections. In the amphibians and
some reptiles some degree of autonomy persists, although in the intact
animal it is masked by the superposition of a control through the nervous
system by means of reflexes originating in the retina. In the frog it has
recently been reported that an intra-ocular reflex occurs — the pupil of the

158

ADAPTATIONS TO ARHYTHMIC ACTIVITY

excised eye contracts somewhat if the retina is stimulated. In the higher
vertebrates, at least in adults, reflexes alone are of importance although
some direct response is known to occur even in two or three mammals
and man; and emotional changes can now affect the pupil, though
whether this is incidental or not, useful or not, is difficult to say. In the
mammals, 'consensual' reflexes from one eye to the other appear: the
movement of both pupils when only one is stimulated (known only in
the rays and the pigeon, outside of the mammals) ; and the neurological
tie-ups of the pupil to accommodation and convergence become rigid.

Fig. 65 — Pupillary opercula in fishes (o- operculum ) .

a, eye of Raja clavata. x 2. After Franz, b, illuminated pupil of R. clavata. After Franz,
c, eye of a flatfish, Scophthalmus rhombus, as seen from above. x3. From Franz, after
Grynfeltt and Demelle. d, upper part of head of stargazer, Uranoscopus scaber. x 4.
Redrawn from Hein. /- lower 'lid'; s- limit of sulcus under lower 'lid', e, f, g, stages in
the expansion of the operculum of a loricariid catfish, Plecostomus. Redrawn from Roth.

Comparative Survey of the Two Methods — In the lampreys there
are no iris muscles and most observers agree that the pupil is static. The
lens touches the cornea and blocks the pupil, and the mechanism
of accommodation (Chapter 10, section A) is such that this relation-
ship is never changed. There are no photomechanical changes in lam-
preys; but their eyes as a whole are built for diurnality. When lampreys
do swim at night, as when going upstream to breeding grounds, they are
in all probability depending upon senses other than vision (like diurnal
birds migrating at night) .

COMPARATIVE SURVEY OF THE TWO METHODS 159

The elasmobranchs are conspicuous among the fishes for having highly
mobile (though excessively slow — v.s.) pupils. The sphincter is unusual
and primitive in that it is never separated from the epithelium which
generates it, as in other vertebrates. They have no retinal photomechan-
ical changes — indeed, no retinal pigment except in the extreme periphery
to which the tapetum lucidum does not reach. Most forms are active
principally at night, but some like to doze, basking, at the surface. A
few may be found active at any hour, and a considerable number live in
the deep sea and are in a constant environment as regards light. The
light-lovers have broadly elliptical, usually vertical pupils which dilate to
circles in low illuminations. The more strongly nocturnal species have
more mobile pupils which close in bright light to narrow slits set diag-

Fig. 66 — Eye of a shark, Squalus acanth-

ias, showing mydriatic pupil rigor, x 1.

Redrawn from Franz.

a, when pupil is freshly illuminated.

b, after illumination of long duration.

/ o/a

Fig. 67 — Dorsal iris-angle region of a teleost,
Chrysophrys aurata. After Grynfeltt.

a- argentea; al- annular 'ligament'; cm-
ciliary muscle; d- dermal contribution to
cornea; i- iris; ip- inner portion of primary
cornea; n- nerve; op- outer portion of pri-
mary cornea; ot- ora terminalis; pc- pars
ciliaris retinae; pi- pars iridiaca retinae; sl-
suprachorioidal lymph space; so- scleral
ossicle; v- blood vessel.

onally or horizontally. They are thus safe from dazzlement and defense-
lessness when they come up to sun themselves. The flattened, upward-
gazing rays are provided with an 'operculum' which can expand to fill
the pupil from within (Fig. 65). The electric ray or torpedo, however,
relies upon a horizontal slit, which a tiny operculum can divide in the
middle. The pupils of elasmobranchs need not necessarily hold their full
contraction in bright light, but are privileged to reopen again after a
time just as though photomechanical changes had taken place — for these
fishes have photomechanical changes in the chorioid which alter the sensi-
tivity of the eye (see Chapter 9, section D) . Some sharks (e.g., Squalus,
Mustelus) in fact develop a 'mydriatic pupil rigor' if kept for several
days in a lighted room — their pupils become widely open and refuse to
close down when additional light is thrown on them (Fig. 66) .

160 ADAPTATIONS TO A RHYTHMIC ACTIVITY

The sturgeons are elasmobranch-like in habits as well as otherwise.
Their pupils (Acipenser fidrescens, Scaphirhynchus platorynchus) are
broad, pointed vertical ellipses or rhomboids, which appear to move only
passively as the lens blocks or unblocks them (in accommodation ?) . The
other chondrosteans, and the holostean fishes, have not been studied.
The lungfishes have no iris muscles although one (Protopterus) has a
mobile pupil. Here the contractility of the unmodified epithelial cells of
the pars iridiaca retinae seems to be involved, as possibly also in a few
teleosts.

Among the teleosts only the eels and the flattened upward-lookers
(e.g., Uranoscopus and Lophius) have much pupil excursion. The com-
mensal pearl-fish, Encheliophis (=Fierasfer) jordani, also has the eyes
aimed upward and is highly exceptional in that its pupils can close to a
mere dot. Many of the flounders and their relatives, and one or two arm-
ored catfishes, have a pupillary operculum (Fig. 65). Most teleosts have
no functional iris muscles whatever, though the non-contractile 'sphincter
of Grynfeltt' is often present. In atypical eyes, like those of Periophthal-
mus, a functional sphincter may be present without a dilatator. The lens
bulges far through the pupil except when pulled backward in accommo-
dation, but does not necessarily actually block it, for in many species
a narrow 'aphakic' (lenseless) space surrounds the lens. The teleost iris
is usually so anchored to the cornea by the so-called annular ligament
(more properly, 'iris angle tissue' — Fig. 67, al) that any iris muscles
would be powerless to alter the pupil. In the minority which do have
iris muscles (and weak annular ligaments) these are peculiar in that the
dilatator consists of true, discrete muscle cells lifted free of the posterior
epithelium and embedded, like the sphincter, in the stroma.

Most teleosts thus depend upon retinal photomechanical changes, which
were evolved by these fishes or by their holostean ancestors. The retinal
movements control stimulation well enough and the animal does not miss
the stopping-down effect of a contractile pupil because of the peculiar
optics of its eye. One would expect the spherical lens to have an excessive
degree of spherical aberration and to need more stopping than the flatter
lenses of terrestrial forms. But the teleost lens has a radially graduated
index of refraction and the retina is a spherical surface, concentric with
the lens. Hence the retina receives a sharply focused image from any
angle and the eye is in effect both periscopic and aplanatic. Constriction
of the pupil would serve no useful purpose. Indeed, the pupil margin
need not overlap the lens at all; and the iris may even be lacking, as in

COMPARATIVE SURVEY OF THE TWO METHODS 161

some deep-sea fishes (Fig. 84c, p. 213), the lens then being huge and
filling the anterior chamber. The teleost pupil may close slightly in
accommodation, probably passively due to its elasticity, when unblocked
by the receding lens; but this is quite meaningless not only because the
lens needs no differential stopping (being fixed in shape), but because
the active accommodation of teleosts is for distant, not near, objects
(see Fig. 98, p. 251).

The pupils of amphibians have more excursion than those of teleosts,
though not as much as they would need if the amphibians did not have
rather good photomechanical changes. Thus the frog, despite its poten-
tially sensitive duplex retina and its extremely large rods (Fig. 64,
p. 148) , has a pupil identical in behavior with that of a pure-cone grass
snake devoid of photomechanical changes. If the frog also lacked retinal
photomechanical changes, his pupil would have to close farther than it
does to permit him to be out where the snake could see him! A few anur-
ans have peculiarly shaped pupils. That of Bombina contracts to a play-
ing-card 'heart'; and in those whose retinae are probably the most sensi-
tive, the spade-foot toads (Scaphiopus spp.), the contracted pupil is a
vertical lozenge, the playing-card 'diamond'. The two other suits of the
deck are apparently not represented among amphibian pupils, but there
are still other weird shapes whose meaning is quite unknown (Fig. 87,
p. 223).

The weak amphibian sphincter pupillae is replaced by a much more
powerful one in the reptiles and here, as in birds also, the iris and ciliary
muscles are of the striated variety. This change may have been inevitable
upon the supervention of a control which is almost completely nervous
and sometimes voluntary, though the return to smooth intra-ocular
muscles in the mammals argues against this supposition. At any rate,
the sauropsidan iris is capable of extremely rapid action, though par-
ticular species do not necessarily ever tax this capacity. The turtle pupil,
fish-like, is blocked by the lens and does not respond to light at
all, contracting only as an accessory to accommodation. Turtles have
practically pure-cone retinae with slight, slow retinal migrations or none
at all. Their insensitive eyes require neither type of protection from
strong light, and in turn limit their possessors to photopic vision and to
dependence upon olfaction in dim light or muddy waters.

In diurnal lizards the iris is but slightly responsive to light, as is true
also of diurnal snakes, some of which have quite motionless pupils.
Nocturnal lizards are usually pure-rod, and nocturnal snakes are rod-

162 ADAPTATIONS TO ARHYTHMIC ACTIVITY

rich or even pure-rod. Many species in both categories are fond of
basking, and the geckoes are often active in the brightest of Hght. This
twenty-four-hour activity is made possible by great pupil excursions,
which are perhaps exaggerated by the absence of movable lids. Thus,
some geckoes if not most or all, and even one or two snakes {Leptodeira
annulata, for example) can close their pupils completely. The gecko,
with a large eye and retinal image, and a retina which, though pure-
rod, often has excellent resolving power (since the rods are but little
summated and owe their sensitivity to their size and to their rich content
of rhodopsin) has probably the best allround, night-and-day eye of
any vertebrate below the mammals.

The crocodile group is nocturnal. Its members, notoriously fond of
basking, depend for the protection of their sensitive duplex retinae upon
the lids and pupil rather than the retinal photomechanical changes, which
are here at a low ebb. Highly active pupils, among the reptiles, thus
go with pure-rod and duplex retinae and are the more mobile, the more
the species or group scorns concealment in the daytime. The circular
pupils of the diurnal majority are relatively or quite inactive, as would
be predicted from their pure-cone retinae.

Bird pupils are very active, but the photomechanical changes have
made a phylogenetic 'come-back' in this group. The paradox is resolved
when one notes the lack of precise adjustment of the avian pupil to
illumination. It plays so much that, although experimental proof is as
yet lacking, many workers have suspected it of being under the bird's
voluntary control. At any rate, it is easy to understand why in the birds
the retina has had to re-assume the responsibility of regulating its own
stimulation — the pupil cannot be trusted to do so.

Mamimalian pupils — except those blocked by enormous lenses in some
strongly nocturnal forms (Fig. 71, p. 173) — are comparable in mobility
with those of birds, but are better-behaved with respect to intensities and
thus make retinal migrations quite superfluous. Excursion is greatest, of
course, in nocturnal forms which love to bask, like the cats and foxes.
It is reduced in many ungulates, and is least in crepuscular forms such as
the bats, in secretive night-prowlers, and in such sun-worshippers as the
ground-squirrels. In short, the more constant are the illumination-condi-
tions in which a group prefers to be active, the less mobility the pupil
exhibits. The pupil closes almost completely in Tarsius, Pedetes, dormice,
and cats, very far in the otters and (by means of an operculum) in some
whales. It has an exceptional range of movement in the seals — but not

DUPLICITY AND TRANSMUTATION 163

primarily, strange to say, for the regulation of intra-ocular illumination.
The unique physiological role of the seal's pupil will be found explained
on pages 446-8.

In the mammals, the retinal photomechanical changes are entirely
gone. In this group of vertebrates we see the end result of the evolution-
ary replacement of those older equalizing devices by the more rapid,
hence highly superior, one afforded by the iris musculature.

(D) Duplicity and Transmutation

The duplex retina itself is clearly an adaptation for the extension of
the seeing-period over a greater number of the twenty-four hours. Rods
and cones are homologous inter se, and one type must have preceded
the other in evolution; for, an intermediate type of visual cell partaking
equally of the qualities of modern rods and cones is quite impossible
of conception.

The accepted belief is that the rod is the more ancient and that the
cone is an improvement upon it; but what real evidence there is points
to the exact reverse of this view. The problem involved here reminds one
of the question: "Which came first, the hen or the egg?" but it is not
without theoretical importance in connection, particularly, with color
vision. The evidence derives largely from the embryology of the visual
cells as interpreted in phylogenetic terms. There is not space here to set
it forth in detail, so the designation of the cone as primitive is bound to
seem a little arbitrary.

Considering the flagellar origin of the outer segment (see Fig. 55,
p. 127) the percipient parts of ancient visual cells must have been
filamentous before they could have become massive, and we cannot
imagine the pro-vertebrate to have possessed already so ingenious a
material as rhodopsin or to have been anything but a strictly bright-
light, pelagic organism. Until some of the visual cells became enlarged,
and grouped in their connections to ganglion cells, there could be no
increase in potential sensitivity which could release the animal from
bondage to the sun; and until the invention of rhodopsin, there could
be no visual activity by moonlight. But withal there must be no whole-
sale conversion of visual cells if the capacity for daytime activity was
to be retained — else the animal would merely have succeeded in shifting
the active period without substantially extending it. Improvements in
the dioptric apparatus making it more and more desirable, for the sake

164 ADAPTATIONS TO ARHYTHMIC ACTIVITY

of form-perception, to retain cones as well as the newer rods, the duplex
retina as we know it today finally crystallized in a condition which made
it possible at last for an animal to become arhythmic if various consider-
ations made that desirable. A mechanism for discriminating hues was
probably added rather late as a refinement whose first purpose was far
from the aesthetic one which color-vision seems, to our anthropocentric
minds, to serve (see pp. 463-4) .

Present-day pure-cone retinae are thus no more primitive than pure-rod
ones, for both represent the secondary discard of a cell type for the sake
of extreme speciaUzations — which, as always, demand in payment the
surrender of plasticity. And, not only have various vertebrates at various
times swung from twenty-four-hour capacity toward diurnality or noc-
tumality, but they have returned from one extreme through arhythmicity
or crepuscularity and even gone on to the opposite extreme.

Wherever even a few cones have been retained in a rod-rich retina,
or a few rods in an almost pure-cone one, manipulations of sensitivity
need be only quantitative and are as readily carried out in evolution as
an alteration of the ratio of white blood cells to reds. But where the
ancestors of a given group retained only one visual-cell type, it might
seem impossible for any descendants ever to produce the other. Exactly
this has happened, however, and apparently far more often among the
reptiles than in any other extant group. Historically, these were the first
vertebrates to feel fully the strain of being highly active without benefit
of a high body temperature. Not only were they deprived of the warmth
of the ancient waters, but they were without the energy-saving buoying
effect which a fish enjoys. A little exertion goes a long way when the
weight of the body is supported by water, and the tenderness of cooked
fish flesh, like that of the disused flight muscles or 'breast meat' of a
chicken, is a reminder of the easy lives such muscles lead.

It is not surprising that in the first terrestrial groups (the stego-
cephalians and the reptiles) many sub-groups tended early to develop
strong diurnality and pure-cone retinae, counting upon the warmth of
the sun to speed metabolism to a degree which would permit of athletic
agility in the search for food. Moreover, diurnality was an especially
safe habit because of the temporary paucity of enemies on land. But the
reptiles have had their heyday and have perforce yielded their place in
the sun to the more successful birds and mammals. Most reptiles are
still strictly diurnal, but as their enemies have multiplied and their
average size has steadily decreased since the days of the dinosaurs, many

DUPLICITY AND TRANSMUTATION 165

have come to be grateful for the shield of night over at least a part
of their activities.

To regain a duplex retina and twenty-four-hour capacity — let alone
to go still further on into nocturnality, loose or strict — the pure-cone
reptiles have had actually to convert or transmute some or all of the
cones into low-threshold, massive, cylindrical elements. In most cases
these have been able to re-invent rhodopsin and thus fully deserve to
be called rods. Intermediate stages in these transmutations can be seen
in living species, which show us therefore some of the steps by which
the original duplex retina may have come into being in the earliest verte-
brates. The conversion of a diurnal reptile into an arhythmic or noctur-
nal one may be illustrated by considering a series of snake species which,
though quite unrelated to each other, each exhibit a stage of adaptation
through which the subsequent members of the series must once have
passed.

All round-pupilled snakes have only cones, of three types as shown
in Figure 26a (p. 63). Two of these are single, one large and abundant
(Type A) , the other small and scanty (Type C) . The third is the unique
double cone (Type B) invented by the higher snakes to replace the lost
double cones of their lizard antecedents (see Fig. 24, p. 59) .

In N. ndtrix, for example, these cone types are normal and typical.
Cemophora is a secretive snake in which the Type A and Type B outer
segments have enlarged, thus lowering their thresholds; but the biggest
change is in the Type C elements. These are no more numerous than
usual, but they have become rod-like in form (Fig. 68a).

The mud-loving and secretive rainbow snakes, Farancia and Abas tor,
maintain the large cone outer segments, and in them the numbers of the
stubby Type C rods have increased until they equal or exceed the total
number of "A" and "B" cones. The Type C elements probably still lack
a rhodopsin at this stage of transmutation.

Any pit-viper, such as Agkistrodon, shows the next logical steps. The
rods have multiplied until they have a human-like abundance relative
to the cones (Fig. 68b) , and they are longer than in the rainbow snakes
and now contain rhodopsin. With this retina, and a small eye with a
small, bright image, the pit-viper has enough sensitivity to require con-
siderable pupil mobility, and the animal can prowl at night and bask in
comfort and safety in the daytime, sometimes even feeding actively then.

From the perfected duplex retina attained in the pit-vipers, among
many others in which this same secondary adaptation to day-and-night

166

ADAPTATIONS TO ARHYTHMIC ACTIVITY

vision has occurred, still further steps may be taken. Thus in Leptodeira
the rods are very numerous, long, and slender, and the bodies of the
cones have gotten up out of their way, their ellipsoids being perched on
the tips of the rods like so many pumpkins on a picket fence (Fig. 69) .
The cone outer segments themselves are very much larger than in
pure-cone diurnal forms like N. natrix, Coluber, etc. Rhodopsin is
abundant in Leptodeira, and the retina is so sensitive that the pupil
closes completely like that of a gecko. In Tarbophis and Dasypeltis the

Fig. 68 — Transmutation in snakes, x 1000.

a, visual-cell types of a secretive colubrid, the scarlet snake, Cemophora coccinea. Compare
Figure 26, p. 63. Types A and B have enlarged outer segments, but Type G (which is
greatly outnumbered by A + B, as in diurnal forms) is the most rod-like of the three.

b, visual-cell types of a crotalid, the copperhead, Aghstrodon mokasen. Types A and B
have remained cones, but Type C (which greatly outnumbers A-i-B) is a perfea rod and
contains a rhodopsin.

cones seem definitely to have lost importance, for while they are still
elongated far beyond the usual position, their bodies and outer segments
are much reduced in size as compared with Leptodeira. In these three
genera (as also, it happens, in the flying-squirrels) the visual cells are in
a condition of 'permanent dark-adaptation' (in terms of the photome-
chanical changes, which do not occur in snakes or squirrels) and the
animals are strongly nocturnal — thus really lying beyond the scope of
this chapter though serving to show the lengths to which a species can
go, if it must, to change its habits and their structural basis.

DUPLICITY AND TRANSMUTATION

167

There are other cases in which nearly all (S phenodon) or absolutely
all the cones of a pure-cone forebear have been transmuted into rods;
and the result is not necessarily a strictly nocturnal animal, for the pupil

O.N.

J

:^ L^rsen

(^ ^ e-G.

G LarsGn
b

Fig. 69^ — Duplex snake retirice. x 500.

a, a nocturnal colubrid, Leptode'tra annulata, whose rods (derived by transmutation from
the Type C cones of a diurnal ancestor — compare Fig. 26) are very numerous, and whose
cones have taken a position which, in terms of the photomechanical changes of lower verte-
brates, might be called one of permanent dark adaptation.

b, for comparison, a boid, Tropidophis melanurus, whose simple, duplex retina is more
ancient than the cone-simplex one from which the Leptodeira pattern was evolved.

C- cone; D.C.- double cone (= Type B); S.- ganglion-cell layer; I.N.- inner nuclear layer;
L.- limitans; O.N.- outer nuclear layer; P.E,- pigment epithelium; R.- rod; S.C.- single
cone (=Type A).

is so well developed in some reptiles that it can often make possible
twenty-four-hour activity even when, behind it, lies a pure-rod retina.
Round-pupilled lizards have only single and double cones, which in

168 ADAPTATIONS TO ARHYTHMIC ACTIVITY

Xantusia have enlarged their outer segments and lost their oil-droplet
pigment. The geckoes have still further enlarged the outer segments,
discarded the colorless oil-droplets, and re-invented rhodopsin. In
Coleonyx, for example, the transmuted rods are enormously long cyl-
inders (Fig. 25, p. 62) and, though sensitive in the extreme, are ade-
quately protected by the slit pupil from dazzlement in the daylight. At
the same time, the rods of Coleonyx are slender enough, and little-enough
summated, to aflFord respectable visual acuity. Thus Coleonyx has been
able to become arhythmic by installing a hinge in the middle of the sensi-
tivity-acuity seesaw. The geckoes can be comfortable in bright light with
a pure-rod retina, while their diurnal lizard relatives, with pure-cone ret-
inae, are completely blind in dim light. It may be a little clearer now, why
diurnality is a more restrictive habit than noctumality; for while a pure-
cone animal cannot see anything, even hazily, at night, a duplex or even
pure-rod species can always see in the daytime, though perhaps not acute-
ly— the real danger being that he will see too much light (bats, owls) if
his share of photomechanical changes, pupil mobility, or lid apparatus is
unable to reduce the stimulation of his rods to a comfortable value.

Pure-rod snakes, as well as lizards, exist by virtue of transmutation. A
few pure-cone ones (e. g. Lampropeltis , Rhinocheilus) have increased
sensitivity somewhat by enlarging the outer segments, eliminating color-
filters (yellow lenses) , and by hooking up more cones to each optic nerve
fiber. Arizona and Trimorphodon have carried these processes so far that
their pupils have had to become elliptical, and in Hypsiglena and Phyl-
lorhynchus (Fig. 26b, p. 63) the visual cells are all morphologically rods
though devoid of rhodopsin. When we can observe so clearly the second-
ary, apparently easy derivation of unquestionable rods from indubitable
cones, it becomes easier to understand why both of these so diverse cell-
types are usually required for a well-rounded visual capacity. And, it is a
little easier to see that in order to become duplex, and thus more widely
useful, the cone-like receptors of the provertebrate retina could spawn
rods without necessity of their having to be formed de novo from a sepa-
rate cellular ancestor. The first rods in the world were produced by the
transmutation of cones, and the process has been occasionally repeated,
wherever needed, ever since the vertebrates came on land.

Chapter 8
ADAPTATIONS TO DIURNAL ACTIVITY

(A) DiURNALITY AND THE EyE

D'turnality and Sharp Vision — The adoption of diurnality entails a
sacrifice of sensitivity. This is hardly possible without a marked increase
of visual acuity, for if the cones are multiplied at the expense of the rods,
resolving power inevitably rises. While it is theoretically possible for an
animal with a pure-rod retina and crude vision to be strictly diurnal,
given the right type of pupil, in actual fact it never happens.

Adaptation to diurnality is thus, at the same time, adaptation for sharp
vision. Diurnal animals are relatively keen-sighted, and their other habits
are such as to demand keen sight; but it is of course impossible in most
cases to say whether they are diurnal and cone-rich in order to have sharp
vision (which is probably true of the birds) or have only cones simply in
order to be diurnal, without making the most of the opportunity to gain
sharp vision (which may hold for the snakes) . The relationship between
visual acuity and diurnality, in so far as it expresses needs and the pro-
duction of adaptations to fill those needs, is perhaps most easily seen in
a rough analysis of feeding habits :

Diurnality, Acuity, and Food — Animals which feed upon small ob-
jects such as seeds and insects must be able to resolve them, which is pos-
sible only for an eye rich in cones and hence diurnal in capacity. Most
lizards, birds, and primates are in this category; as are also the tree-
shrews, at least, among the insectivores. It is important to remember that
insects themselves are poikilothermous, hence most species are most active
and available under diurnal conditions. Nocturnal insect-feeders can
place no reliance upon vision, but must either rely upon hearing and
touch for securing individual insects (bats) or else 'trawl' blindly through
the air for flying insects with wide-open mouth (goatsuckers, frog-
mouths) . The dependence of most birds upon sunlight is proverbial. So
is their visual acuity. In this respect, man acknowledged even the small
birds to be his superior, centuries ago — it was the habit of the medieval
falconer to carry a caged shrike on his saddle, to keep track of the falcon.
As long as the shrike acted fearful and excited, the hawker knew that his
proud tiercel was in sight — though not to him\

169

170 ADAPTATIONS TO DIURNAL ACTIVITY

Poikilothermous vertebrates, generally, may be diurnal for the sake of
the activating effect of sunlight upon metabolism and locomotor activity,
unless they happen to be particularly defenseless or especially dependent
upon prey which in itself is nocturnal. Predaceous fishes, most reptiles,
and some frogs fall here.

Predaceous vertebrates, generally, require fairly sharp vision at rela-
tively close range in order to pursue and capture prey and obtain a grasp
upon it which will be advantageous to them in any ensuing combat. Be-
ing ordinarily swifter than the prey — at least for short bursts — there is
added need for acuity of vision, which must keep pace with speed if
'crashes' are to be avoided. These factors are especially operative in
fishes, lizards, and birds; and they are largely responsible for the acuity-
adaptations tenaciously retained by those carnivorous mammals which
attempt to compromise between sensitivity and acuity by having large
eyes. Small, small-eyed carnivores on the other hand are nocturnal,
largely because the small prey animals which they are able to master
have taken refuge from them in nocturnality.

Defenseless, herbivorous prey animals which rely upon speed for escape
must recognize enemies at a distance. This in itself demands high visual
acuity; and the factor of distance, besides reducing the retinal-image size
of the potentially dangerous object seen afar, greatly reduces its bright-
ness. Vision at a distance is therefore altogether impossible in dim light.
The ungulates, and the more strictly diurnal mammals, must have high
visual acuity for safety, and their acuity-devices will work only under
bright-light conditions. Lastly, predators which specialize on diurnal prey
must ordinarily be permanently or temporarily diurnal themselves — the
hawks, for example, as also the bear during his annual gorge on salmon.

However, we must not suppose that in every act of predation both par-
ties are under optimal conditions and fighting to best advantage. On the
contrary, many a predator is nocturnal in order to seek out prey which,
being itself diurnal, is asleep at night and hence at a disadvantage. Con-
versely, the diurnal predator may depend not upon diurnally active food
animals, but upon nocturnal ones which, sleeping in their burrows by
day, are then easily surprised and subdued. The diurnal snake exploring
the nests of slumbering rodents, the nocturnal marten investigating a
squirrel's dray, are examples of these advantageous employments of the
sleep-time of the victim.

We can easily imagine that diurnality and nocturnality have come and
gone, sometimes repeatedly, in particular lines of descent. Prey animals

DIURNALITY, ACUITY, AND FOOD 171

have become nocturnal to avoid predators. Predators have in turn be-
come nocturnal to continue to find food easily. To escape the nocturnal
predators, prey animals have again become diurnal. Those species and
groups which could not invert their habits at need were doomed unless,
by sheer weight of numbers, by phenomenal fecundity, they were able to
compensate (as species) for the enormous losses of ill-equipped indi-
viduals.

The Eye as a Whole — For an eye to mediate sharp vision, an essential
requirement is a large retinal image. The greater the number of visual
cells over which the image is spread, the greater the resolution of the de-
tails of the image. The histology of the retina is a very important factor
but, after all, it can only say the last word in the story the eye tells the
brain. There are strict limits to the fineness of the receptor mosaic, and
its performance is in turn limited by the size of the image presented to it
by the dioptric apparatus.

The simplest way to gain a large image is to have a large eye; and
'large' here refers to absolute, not relative, size; for whereas with other
organs of the body it is relativity to each other that determines adequacy
of size, the eye is essentially an optical instrument and obeys the laws of
inter-organ proportioning only grudgingly, disobeying them entirely
whenever, with impunity, it can. Biologists tend to overlook this fact, and
frequently remark of large animals, such as the whales, that "their eyes
are so small in proportion that they must be just about useless"— forget-
ting that the world looks the same size to a whale, a man, and a mouse.
They all see as much, but not as well. Were a squirrel as big as a horse,
it would have an eye as big as a horse's; but that is not to say that if a
horse were as small as a squirrel, it would see as well with an eye propor-
tionately small. The squirrel would, on the other hand, be much better
off with eyes as big as a horse's — if it had room for such eyes in its head.

The big reason for this fact — that it is absolute rather than relative size
which, ceteris paribus, determines visual acuity — is that the absolute
dimensions of retinal elements vary within only narrow limits however
large or small the eye may be. Tripling the diameter of the eyeball does
not entail tripling the diameter of a cone visual cell. Rather, it results in
a tripling of the number of visual cells in a given linear distance on the
retina. The image is then three times as broad, and visual acuity is en-
hanced threefold.

In practice it is only exceptionally that high visual acuity can be gained

172

ADAPTATIONS TO DIURNAL ACTIVITY

merely by having a large eye whose parts are proportioned as they are in
small twenty-four-hour eyes. It is only in large animals such as the ungu-
lates and the great cats that we find high visual acuity attributable prin-
cipally to large ocular size as such.

Where the habits of the animal demand that he go all out for visual
acuity, we find the eye to be large both absolutely and relatively. Thus in
the birds the eyes are proportionately colossal and occupy so much of the
head (Fig. 70) that their fundi may actually roll upon one another in

Fig. 70 — Eyes and brain of the English sparrow, Passer domesttcus, in situ, from the ventral
side. X 5^^. Redrawn from Wood and Slonaker,

c- optic chiasma; e- external rectus; g- Gasserian ganglion; h- Harderian gland; in-
inferior rectus; io- inferior oblique; ir- internal rectus; /- lacrimal gland; m- medulla;
o- optic nerve; ol- optic lobe (midbrain); p- pituitary; 5- third cranial (oculomotor)
nerve — supplies the superior, internal, and inferior reai and the inferior oblique; 4-
fourth cranial (trochlear or pathetic) nerve — supplies the superior oblique; 5- fifth cranial
(trigeminal) nerve, several of whose branches carry fibers to the eye and adnexa; 6- sixth
cranial (abducens) nerve — supplies external reaus.

the mid-plane of the skull, like a pair of segmental gears. Only in species
of little brain can such things be.

The partial dependence of resolving power upon absolute ocular size
has a consequence upon relative ocular size. It has been stated as a law
that eye size is inversely proportional to body size (Haller's ratio) . The
reason why this should hold for nocturnal forms as well as for diurnal
ones will be given in the next chapter; but it is a very different reason.
Keeping only diurnal forms in mind, it is easy to see why the eye should

THE EYE AS A WHOLE

173

be relatively large in, say, small birds and yet relatively small in such an
animal as the horse. Though the horse has larger eyes than any other
land mammal, there is ample room for even such large eyes in the head.
The small bird must give over a far greater proportion of the head to the
eyes if they are to be large enough in actual measurement.

NOCTURNAL:
5

ARHYTHMIC:

DIURNAL-

Fig. 71 — Intraocular proportions in relation to intensity habits.
Redrawn from various sources.

inferior side of eyeball; n- nasal side; s- superior side; /- temporal side.

Another factor which, by operating upon actual ocular size, has its
effect upon relative ocular size, is locomotor speed. Great speed demands
high resolving power for better perception of movements and for the
avoidance of collisions (Chapter 10, section E) ; and this calls for a large

174 ADAPTATIONS TO DIURNAL ACTIVITY

eye. In predaceous fishes, lizards, birds, ungulates, squirrels, and other
swift and agile forms, large eyes go with swiftness of movement (Leuck-
art's ratio).

Wherever the eye of a diurnal animal is actually small it may be that
visual acuity is low because, considering the animal's habits and needs,
it need not be any higher. This is the situation in the snakes. Far more
often, the eye is small because there is simply no room for a larger one.
Internal adaptations then appear, which compensate for inadequate size;
and the same adaptations occur in even very large eyes, supplementing
the effect of size per se, wherever maximal visual acuity is desired.

These internal rearrangements usually consist at least of a flattening
of the lens and a shallowing of the anterior segment of the eyeball. (It
should be remembered that the anterior segment is not defined as the an-
terior halj of the eyeball, in front of the equator, but as the portion anter-
ior to a plane tangent to the back surface of the lens. This may com-
prise very much less than half of the volume of the eye). These changes
have taken place in the birds and are perhaps most marked in the
chameleon and in the higher primates (Fig. 71). The squirrels are
conspicuous for having more nearly spherical lenses than other strictly
diurnal vertebrates. The human eye, among mammalian eyes in gen-
eral, is atypical in the other direction, in its possession of so very flat
a lens. One gets the impression from the human, as also from most bird
eyes, of an ordinary-sized anterior segment grafted onto an oversized
posterior segment which 'doesn't belong' to it. This impression is actually
quite true to the facts, for it is not that the parts of the anterior segment
have been made smaller in order to gain visual acuity, but rather that the
fundus of the eyeball has been made larger, the lens then flattening in
order to move the focal level back onto the now more distant retina.
The fishes are peculiarly fortunate in that they are able, because of the
extraordinarily high refractive index of the lens, to obtain a broad image
without the eye having to be as deep as it is broad. The fish eye is con-
sequently flattened (Fig. 77b, p. 185) and encroaches less upon the in-
ternal structures of the head.

The effect of this alteration of the relative size of the anterior and pos-
terior segments is to move forward the nodal points of the dioptric sys-
tem. The distance from the optical center to the retina being thereby in-
creased, the image enlarges just as it does when we draw a stereopticon
lantern farther away from its screen. For the greater distance of 'throw'
of the image, the lens must now bend the light-rays less sharply if they

THE DIURNAL RETINA 175

are still to focus on the retina; hence the reduction of its sharpness of
curvature. If we imagine the acuity-requirements of an animal to be stead-
ily increasing through evolution, we may visualize the consequent gross
changes in the eye thus :

1. A steady increase in absolute size until the eye is relatively large
if the animal is small. If the animal is large, the eye may then still be
relatively small though absolutely large. The result is an enlargement
of the image and an increase in resolving power since the visual cells do
not enlarge proportionately, but instead become more numerous per
angular unit of the image.

2. A faster growth of the fundal portion, the anterior segment be-
coming, more and more rapidly, relatively small as compared with the
posterior. The result is an increase in the size of the image relative to
the size of the eye, with a consequent increase in resolving power.

3. A relative or an absolute forward movement (or both) of the
optical center of the cornea-lens system, further expanding the image
owing to the increased distance from optical center to retina (Fig. 71).

4. A relative diametral shrinkage and flattening of the lens or the
cornea (or both) , increasing the focal length to suit it to the increasing
distance from optical center to retina.

5. A relative diminution of the size of the pupil and of its excursion
of movement, there being abundance of light entering the eye under
diurnal conditions (so that the pupil can be small) and, in the pure-cone
retina in which diurnality tends to culminate, a restricted range of sensi-
tivities (so that there is no point to having the pupil capable of opening
very widely or of closing extremely) .

(B) The Diurnal Retina

ConeiRod and Receptor:Conductor Ratios — The diurnal retina is
invariably rich in cone-substance. This clumsy term must be used in at
least this one place, for the sake of emphasizing that it is the relative
total masses, not the numbers, of cones and rods which count in retinal
adaptations to sensitivity. For, an animal may have dozens of rods to
every cone and still be suited best for diurnal activity — if the rods are
tiny and the cones massive. This is actually the case in the bright-light
teleost fishes (Fig. 22b, 23c, p. 54). Apart from them, the rule is that
relative numbers of cones-per-rod are high in diurnal forms, low in
nocturnal. And within the teleost group, this rule of numbers of course

176 ADAPTATIONS TO DIURNAL ACTIVITY

holds. Wunder made counts in a number of species, and found the
greatest number of rods (810,000 per square miUimeter of retina) in the
nocturnal Lota. Lota also had the fewest cones (3400/sq. mm.), the
diurnal Tinea the most (9000/sq. mm.). The catfishes, however, have
thick rods in their crude eyes. Wunder found no other teleost with so
few rods as Amieurus (l8,400/sq. mm.), whose rods are almost am-
phibian in plumpness (c/. Figs. 63 and 64, pp. 147-8) .

The most strictly diurnal vertebrates have only cones in their retinae.
Among these are the great majority of lizards and snakes (all of those
with round pupils), some (perhaps many) birds, and the majority of
the members of the squirrel family — at least, the marmotines (ground-
squirrels, prairie-dogs) are certainly pure-cone, and all others except the
flying-squirrels are probably pure-cone.

In many birds, only a few rods can be found and these may be
present over only a part of the whole retinal area. Cones outnumber rods
very greatly in all diurnal birds which have any rods at all. Turtles have
very few rods among their cones, and some species may have none. In
freshwater lampreys, the cones and rods are equal in numbers; but in
marine species the rods are more numerous to give the added sensitivity
demanded by deeper water.

The most nearly diurnal of the amphibians — the frogs — have much
higher cone-to-rod ratios than do some vertebrates which are more
strictly diurnal than they; but in the amphibians the rods are so large
and the cones so small that we have here a situation which is the reverse
of that in the teleosts. The actual effect is of a preponderance of rods —
just as in teleosts, with the rods very numerous but very tiny, there is
an effective preponderance of cone-substance.

Except for the vertebrates above-mentioned, none is known to exceed
by very much the cone-to-rod ratio of man, which is about 1 : 20 and
seems very low — until we take account of the great size of the eyes of
primates, large carnivores, and ungulates, whose retinal image sizes are
such that many rods may be allowed to leak in between the cones with-
out the visual acuity being pulled down below that of a small bird whose
retina is pure-cone and whose cones are contiguous. Thus, where an
animal has room for a large-enough eye, he can afford to have a duplex
retina without sacrificing too much visual acuity, and then has the
opportunity of seeing something in twilight or moonlight, whether he
takes the opportunity or not. Most do — and thus it is that ungulates,
large carnivores, and primates are able to stay up after the birds have

THE DIURNAL RETINA

177

gone to bed, and tend toward twenty-four-hour activity. The presence
of enough rods to make this possible would sometimes affect visual
acuity too adversely, except for the development of a small pure-cone
area, the 'area centralis', in the otherwise duplex retina. Such an area,
like the whole of a pure-cone retina, is necessarily blind in dim light.
The outer nuclear layer, formed by the rod and cone nuclei, tends to
have few rows in diurnal retinse. Cones being usually more plump than
rods, there is more room for their nuclei to lie directly against the ex-

|Diurnal|

receptors '

(many cones)

summoted

but little

in:

BIPOLAR CELLS-^

finally
sunnnnated
but little
* in:

GANGLION CELLS*

-•-BIPOLAR CELLS

nally

summated

extensively

in:

GANGLION CELLS

Fig. 72 — Diurnal and nocturnal retinae contrasted.

The diagrams represent two related species, one of which is diurnal and the other noaurnal.
The characteristic differences in the relative thickness of the nuclear layers are the result of
the visual-cell patterns and the differing extents of summation in optic nerve fibers.

ternal limiting membrane. Where rods are few or absent, this makes for
a thin outer nuclear layer. In some lampreys, there is but a single row
of nuclei. Turtles and squirrels have but a couple of rows, as do the
amphibians — in the latter it is the unusual bulk of the rods, and their
relatively small numbers, which is responsible. Where the rods are
slender and are as numerous as they are in man, the outer nuclear layer
becomes thick; and (Fig. 69a) it becomes far thicker still, of course, in
twenty-four-hour and nocturnal eyes (except, again, in amphibians) .

178 ADAPTATIONS TO DIURNAL ACTIVITY

Where the cones are slender, hence numerous per unit of retinal
area, their nuclei pile up in several layers. This is true in lizards and
particularly in birds; and in all cases, in the pure-cone spots in duplex
retinae referred to above and treated at length in the next section. The
snakes are quite conspicuous, among pure-cone forms, for having single
outer nuclear layers — the reason being that the cones are generally fatter
than their own nuclei (Fig. 68) , since only a few snakes (e.g., Dryoph'ts,
Malpolon, Sepedon) have taken advantage of their diurnality to obtain
high visual acuity by slenderizing their cones.

Though the outer nuclear layer tends to be thin, the inner nuclear
and ganglion layers tend to be thick in diurnal animals. This is an
expression of the reduction of summation (see pp. 47, 67) , of the increase
in the number of neurons per number of visual cells, for the preservation
of the high resolving power which the multiplication and slenderization
of the cones tends to produce. A diurnal retina can thus often be dis-
tinguished at a glance from a nocturnal one, for in the former the inner
nuclear layer is usually thicker than the outer, this situation being re-
versed in the nocturnal retina (Fig. 72). A considerable portion of the
characteristic thickening of the inner nuclear layer of diurnal retinae is
due to the greatly increased numbers of horizontal and amacrine cell-
bodies ; for, as diurnaUty is adopted and perfected by a vertebrate group,
these integrative cells are multiplied even faster than the straightforward
conductive ones (bipolars and ganglion cells) and may, as in birds,
come to outnumber the latter. Though it would seem that ganglion:
bipolar: visual-cell ratios would take up and finish the job of fixing
visual acuity where the size and quality of the image and the concen-
tration of cones leave off, the 'switchboard' effects of the horizontally in-
tegrative neurons have a mysterious and very considerable concern with
the sharpening of the mental picture, probably by manipulating contrast
phenomena. This particular specialization makes the bird retina the
thickest of all— though it should not be thought that the variation of
retinal thickness from group to group of animals is a very great one,
for it is surprisingly slight.

Minimization of the Physiological Scotoma — The 'blind spot' of
the retina may, in thoroughgoing diurnal eyes, be called upon to modify
itself in sympathy with the efforts toward improving detail- and form-
perception. The insensitive head of the optic nerve, called the 'disc'
from its usual appearance when seen with the ophthalmoscope, causes

NULLIFICATION OF THE BLIND SPOT 179

a physiological (normal) scotoma or gap in the visual field within which
nothing can be seen. We humans are not aware of our blind spots, for
since the two retinal topographies are mirror-images of each other and
both are aimed forward, any object whose image falls within the disc of
one retina is simultaneously imaged upon functional retina in the other
eye. We are not even aware of the blind spot when one eye is kept
closed, and can demonstrate it to ourselves only in an experiment such as
is shown in Figure 73. An animal whose eyes are on the sides of his
head, however, might as well have one eye closed so far as concerns what
the other fundus is seeing; and hence he cannot fill in, with each eye,
the blind spot of the other.

The blind spot becomes a serious matter only where the disc is rela-
tively large; but this happens to be inevitable when the eye is especially
well adapted for diurnality. For, it will then have a preponderance of
cones, and the consequent great numbers of ganglion-cell axons make
for a relatively heavy optic nerve and a large disc. On the other hand,

Fig. 73 — Demonstration of the blind spot.

Cover the right eye; fixate the star steadily and move the book slowly toward and away
from the face. The words at the left will disappear and reappear as their image swings
on and off of the head of the left optic nerve.

the disc of a mouse is a mere dot, for each of the few optic nerve fibers
is connected with hosts of rods.

In three diurnal assemblages the disc has become a narrow, greatly
elongated oblong : in the squirrels, the birds, and the predaceous pikes,
salmonoids, and percoids among the teleost fishes. Elsewhere it is usually
circular but it may be oval, reniform, triangular — always, however, com-
pact. A fatally large, compact disc has been avoided in the fishes by
permitting the developing optic nerve fibers to fill in the whole length of
the embryonic fissure of the optic cup, instead of massing them at the
apex of the fissure (see p. 108) as other vertebrates do. The optic nerve
thus often departs from the fish eyeball as a ribbon rather than a cord,
and becomes crumpled edgewise to gain a circular cross-section between

180 ADAPTATIONS TO DIURNAL ACTIVITY

eye and brain (Fig. 105e, p. 261). In the birds, the stripe-like disc is con-
cealed under the base of the 'pecten', a pleated fin of pigmented, highly
vascular tissue which arises embryologically from the lips of the embry-
onic fissure and projects lens-ward through the vitreous (Fig. 80, p. 188).
The birds thus have only one narrow scotoma where they might have
had two if they had located the pecten elsewhere.

The squirrels exhibit the most remarkable of all modifications of the
disc (Fig. 74). It is a stripe, oriented horizontally to interfere minimally
with the perception of vertical contours which are so important to an
arboreal animal. It has been moved far above the optic axis whereas in
other vertebrates it is almost invariably located close below the axis or
even on it, in the center of the fundus. Since it is the lower part of the

Fig. 74 — The optic disc in various members of the squirrel family.

(In schematized views of the fundal portions of left eyes, the anterior segments being cut
away; the drawings are not to the same scale).

a, prairie-dog, Cynomys ludoyidanus (inhabits open spaces, very bright light), b, wood-
chuck, Marmota monax rufescens (inhabits less bright places), c, gray squirrel, Sciurus
carolinensis leucotis (inhabits dense woods), d, flying squirrel, Glaucomys v. volans (noc-
turnal, with a nearly pure-rod retina).

retina which looks upward, vision of the sky, where the squirrel's chief
enemies soar, is thus left unimpeded. The stripe-like disc is so slender
that it bites out only tiny bits of vertical lines; and a tiny head or eye
movement, up or down, will move any horizontal line off the disc and
onto functional retina. Where the number of optic nerve fibers varies
from species to species, the stripe varies in length (but not in width),
in sympathy with the species' preference for bright light — from 7%%
of the diameter of the eye in the sun-worshipping ground squirrel
down to 30% in heavy-timber tree squirrels and even less in the Eu-
ropean squirrel (where also it widens somewhat) , which seeks the darkest
woodlands. The palm squirrel and the nocturnal flying-squirrels, as
might be expected, have perfectly orthodox small, circular discs located
just below the center of the fundus.

ARE/E CENTRALES AND FOVEJE 181

(C) Are^ Centrales and Fove^

The Area Centralis — An important feature characteristic of the best-
adapted diurnal eyes, and found in many twenty-four-hour eyes (as an
adjunct to their diurnal activity phase) is the area centralis. It is best
defined as a circumscribed retinal area within which the retina is so
constructed as to afford a marked local increase in resolving power.

The name 'area centralis' is not too fortunate, for the area is not
necessarily near the center of the fundus — though it happens to be in
man, whose morphology has greatly influenced all anatomical termin-
ology. In the human and other primates, the macula lutea (= yellow
spot) of the retina is synonymous with 'area centralis', but the term
'macula' is most improperly applied to the areae of other vertebrates.
Similarly, the word 'fovea' is often badly misused, and it will be well
to get these three terms firmly and accurately in mind :

An area centralis is only exceptionally pigmented, making of it a
yellow spot on the otherwise colorless retina. Only then can it properly
be called a macula lutea. This latter term should consequently be re-
served— if, indeed, there is any need for it at all — for the areae centrales
of the higher primates, and possibly the chameleons. No others are
known to have the diffuse yellow pigmentation of the inner layers of the
retina in the area centralis.

Again, only certain areae centrales have a depression or pit in the
center; and it is just this pit, not the whole area, which should be called
a fovea. An area centralis can occur without a fovea — it may actually
be thickened, not thinned — but a fovea can exist only within an area
centralis.

The various features of a full-fledged area centralis can best be set
forth if we enumerate them as steps in the evolution of such an area in
a hypothetical vertebrate. This animal must have taken on diurnality
and — unless of course he eventually dispenses with rods entirely — must
have a large-enough eye to be able to afford to devote a portion of the
retina to an area centralis without sacrificing the ability to see in dim
light with the greater part of the retina.

The first obvious thing to do is to increase, locally, the number of
visual cells per unit area of the retina. This is brought about partly by
making them more slender, partly by packing them more closely to-
gether than they are outside the area. Since the rods are like so much
deadwood when it comes to affording highly-resolved images to the

182 ADAPTATIONS TO DIURNAL ACTIVITY

consciousness, they are progressively eliminated and the area comes to
be a pure-cone island in a duplex sea of unmodified retina.

As the rods are eliminated and the cones are aggregated and slen-
derized, the threshold of stimulation of the area tends to rise. The
areal cones would then go out of action, in failing illumination, before
the more massive extra- areal ones; but they counteract this tendency by
evolving longer and longer outer segments. This local thickening of the
visual-cell layer causes the external limiting membrane to bulge inward
toward the vitreous, and may even make the pigment epithelium bulge
outward against the chorioid ('fovea externa'). Retinal blood vessels,
where these are present (mammals) tend now to be excluded from the
area so as not to interfere with clear perception, and the chorioid may
have to thicken locally to carry the extra nutritional load. The increased
length of the visual cells has a fortuitous but very fortunate effect upon
the burden carried by the mechanism of accommodation (see pp. 30-1).

a

Fig. 75 — Well-developed (avian) and poorly-developed (human) iovex. x 271/2.

Cross-hatched in each diagram is the portion of the foveal retina which is actually thinner
than the retina outside the area centralis. The superior avian fovea is less a 'thin spot' than
is that of man. a, foveal region of hawk, Buteo b. borealis. b, macular region of normal
human retina.

The increase in the percentage of cones results in a great increase
in the number of bipolar and ganglion cells, since cones are summated
less in them to begin with, and less within the area than outside of it
— each cone, ideally, coming to have its own bipolar and ganglion cell
transmission-line to the brain.

The thickenings of the visual-cell, outer nuclear, inner nuclear, gang-
lion-cell, and nerve-fiber layers add up to a local thickening of the retina
as a whole. Where this might become extreme, a fovea develops — not
to combat the thickening as such, but rather the convex surface thereof
which bulges into the vitreous.

The Forea—The reader, stopping at any point in the above discussion,
would then have already read a complete description of some area cen-
tralis which actually exists in some vertebrate or other. Most arese do
not go on to develop a fovea, and fewer still of these have produced the

ARE^ CENTRALES AND FOVE/E

183

local yellow pigmentation which creates a macula lutea and is a final
refinement in making the area centralis the spot of maximal visual acuity.
For the full comprehension of the meaning of the foveal depression we
must revert for a moment to the elements of physiological optics.

A light ray passing through the cornea and lens and striking the
retina perpendicular to its surface will travel on through the retina with
its direction unchanged. It was long thought, however, that an appre-
ciable amount of the light would be absorbed and scattered in the retinal
tissue before reaching the visual-cell layer, thus not only being lost for
purposes of image-formation but, more important by far, tending to
blur the image. The depression of the fovea was then thought of as a
thin spot produced for the sake of thinning, and serving to remove tissue

vitreous

vitreous

Fig. 76 — Local magnifying action of the foveal depression (based on the
central fovea of a hawk, Buteo b. borealis).

from in front of the important central bouquet of cones in the area. This
theory must be discarded however, for in the best of areae (in lizards and
birds) the portion of the depressed retina, which is thinner than the
retina outside the area, is smaller than in arex with shallow foveas which
are known to be degenerate (Fig. 75). The retina, in life, is completely
clear and actually extinguishes no more light than the same thickness of
vitreous — which, of course, fills in the foveal excavation.

A clue to the real meaning of the fovea (Fig. 76) was made available a
half-century ago in some observations of Valentin on the refractive index
of retinal tissue; but, it went unrecognized as a clue until very recently.
The data never seemed of any possible usefulness, and one finds no
figures given in modern reference books. But the index of the retina was

184 ADAPTATIONS TO DIURNAL ACTIVITY

carefully measured by Valentin in a number of animals and was found
to be always substantially higher than that of the vitreous. What this
means is that if a light ray should strike the vitreoretinal boundary at
anything but a right angle it will be refracted away from an imaginary
perpendicular to the surface at the point of its impact.

The foveal depression is designed deliberately to take advantage of
this refraction. The foveal portion of the retinal image is expanded on
its way through the retinal tissue, and is thus magnified somewhat when
it reaches the level of the visual cells. In birds the magnification is about
13% linearly, 30% in area; and it is probably greater in lizards. The
linear increase directly affects visual acuity. The areal increase improves
the perception of 'pattern', though it adversely affects sensitivity to
external illumination. A part of the lengthening of foveal cones, two
advantages of which have already been mentioned, is perhaps in com-
pensation for the local dimming of the expanded portion of the image.

When an area centralis has done everything else possible to increase
the number of receptor-units over which the image will fall, the further
increase afforded by a deep fovea makes the production of one decidedly
worthwhile — nay, mandatory, for the convex bulge in the internal limit-
ing membrane over a highly-developed area centralis would tend to
converge the rays of light and make the image, at the level of the visual-
cell layer, smaller. The shallow depression in the area centralis of a soft-
shelled turtle (Fig. 78b) or the average teleostean fovea probably does
little more than cancel the minifying effect of the area's convex inner
surface. The deeper the actual depression goes below the original level
of the retina, the higher the mound or 'circumfoveal eminence' created
around the depression by the displaced tissue. Since a continuous steep
slope is thus produced from the crest of the mound to the bottom of the
depression, this sloping surface becomes an effective magnifying device,
of optically unique description.

Distribution — No lamprey has an area centralis, but one occurs in
Mustelus — the only genus of sharks known for certain to have any
cones at all. It is marked by a noticeable concentration of ganglion
cells (Fig. 77a). An area centralis is very commonly seen in bony fishes,
and a fovea (Fig. 77b) has been found in a score or so of teleosts (see
Table III, p. 187) , never as deep as in lizards but with both rods and twin
cones excluded from it. The areae centrales of frogs, most turtles (Fig.
78), and all crocodilians are devoid of foveae and are imperfect in that
they contain rods as well as cones— indeed, the crocodilian is nocturnal

ARE^ CENTRALES AND FOVE/E

185

and it is more than likely that its area centralis is an area of especial
sensitivity, not of acuity at all.*

In only two genera of snakes is a fovea positively known to occur.
The East Indian long-nosed tree-snake, Dryophis mycterizans (Fig. 79)
has a keyhole-shaped pupil with the slot of the keyhole pointing forward
well beyond the rim of the lens, thus constituting an extensive aphakic
space. The fovea in Dryophis is at the outer rim of the retina on the
temporal or caudal side of the eye, and a line from it through the center
of the lens passes out through the slot in the keyhole pupil, along a
groove on the cheek in front of the eye, and straight forward parallel
to the axis of the body. It is significant that herpetologists have long

Fig. 77 — Area centralis and fovea in fishes.

a, portion of retina from sagittal section of eye of a shark, Mustelus mustelus. After Franz.
ac- area centralis (note increased length and concentration of visual cells, number of
ganglion cells).

b, eye of a teleost, Serranus scriba, horizontal section; retina shown in black. After Kahmann.
/- fovea; n- nasal side; ^ temporal side.

*The same suspicion falls upon the ungulates and carnivores, hardly any of which are
strictly diurnal. The majority of afoveate arese would in faa bear re-investigation with this
suspicion in mind, for it is already known that the special area of the opossum has its
histological peculiarities aimed at increasing sensitivity, not resolving power. There appear
to be circumscribed central areas of extreme sensitivity in the retinje of the echidnas and
some 'edentates', for these nocturnal animals are reported to wince and close their eyes in evi-
dent distress whenever the light-beam of an ophthalmoscope strikes the small area mentioned.
This, by the way, is quite a different thing from the phenomenon in the human eye which
has led some careless ophthalmologists to refer to the macula lutea as the 'most sensitive'
spot in the human retina. It is the least sensitive spot, becoming quite blind in low illumi-
nation— but it happens to be the pupillomotor area, the part of the retina which controls
reflexly the closure of the pupil when illumination is suddenly increased. The fovea of the
owl is also the pupillomotor area — and here, perhaps, it is extremely sensitive as well, in
the true sense of 'sensitive'.

186

ADAPTATIONS TO DIURNAL ACTIVITY

been in agreement that this snake has the sharpest sight and the most
accurate judgment of distance of any in the world. A very similar situa-
tion obtains in the African bird snake, Thelotornis ktrtlandi; and prob-
ably also in Dryophiops, whose pupil is similar.

a in turtles.

sagittal section of retina through the area centralis of the western painted turtle, Chrys-
emys picta marginata. The optic nerve head is out of the picture a bit to the right,
b, section of retina through the fovea of a soft-shell turtle, Amyda sp. Redrawn from Gillett.

pe- pigment epithelium; r- receptor layer; /- limitans; on- outer nuclear layer; op- outer

plexiform layer; in- inner nuclear layer; ip- inner plexiform layer; g- ganglion layer; n-

nerve fiber layer.

Fig. 79 — The East Indian long-nosed tree-snake, Dryophis mycterizans.

a, right eye in situ, from the side, showing aphakic portion of pupil and cheek groove which
permits straight-forward vision, x 4. From alcoholic specimen, as- aphakic space; /- lens;
g- groove, b, face, showing provisions for binocular vision, x 2. From Franz, after Beer,
c, anterior segment of right eye, showing form of iris, lens, and aphakic space, x 4. From
Franz, after Beer, d, head from above, cut away to reveal eye in section, showing line of
sight from temporal fovea through lens and aphakic portion of pupil and along cheek
groove, x 2. From alcoholic specimen and microscopic preparations.

TABLE m-AREAE AND FOVEAE

AREA

FOVEA

CO

u

I

CO

Ll.

Cyclostomes

Elosmobronchs

Mustelus only;
central and round

ChondrDSteans,HolosteGns,Dipnoans,aadistians

Teleosts

Many

temporal; poorly
defined at best

Bothy frocfes (deep-sea)
has pure-rod fovea

A few littoral marine spp.

temporal (nearly cen-
tral in HipDOcampus)

shallow to medium
(deeo in Gire/lo sp.l)

AMPHIBIANS

Anurans

crescent over _^

ODtic DODilla-. ^T^

Urodeles and
Ccecilians

REPTILES

Sphenodon

central

medium (pure-rod!)

Crocodilians

horizontal band (prob-
ably not an acuity area)

Turtles

central, round

Amyda only; shallow

Lizards

Nocturnals

Diurnals

central; round or oval
(temporal in Voranus)

deep (shallow in large
skinks and Voranus)

Snakes

Nocturnals

Diurnals

temporal; poorly defined

Dryophis, Dryophiops,
and TheloforniS; medium

CO
Q

CD

Most (including most vultures?)

central, round

medium to deep

Some ground-feeders; domesticated spp.

round, poorly defined
at best; often absent

pigeons only
(shallow and variable)

Some ground -feeders; many
swimmers, divers, and waders

central and round, set in
horizontal band which is
also organized for acuity

r

nedium,in round orea^

t

Hawks, eagles, swallows, terns

two circular, fovea te '"

areas connected by -

horizontal band--

^^=- (terns. =«°) '

o
>

two- central (deep) &
temporal (usually med-
ium, but is the deep-
er of the two in eaales)

Kingfishers, bitterns, humming-birds,
some wing -feeding passerine spp.

two: central and ten> ■
poral, both round, not
connected by a band

two; central (deep)
temporal (medium)

Some gulls, shear -waters, flamingo

horizontal bond

linear (trough-like) fovea

Owls, Apus apus, Sfrigops habroptilus

temporal, round (a fain
central one also in /I/^5

shallow; sometimes none

MAMMALS

Most

Ungulates

more or less temporal; us
ually broad horEontal banc

Carnivores (espec. felids)

central, compact

Sguirrels(espec marmots)

horizontal bond,
not well defined

Primates

Lower
(and Aotus)

Lemur cgtfa,L.macoco
and Aofus only; centra

Higher

central , round

deep but broad in man
(more abrupt in some?)

187

188 ADAPTATIONS TO DIURNAL ACTIVITY

In lizards the area is central, and is circular or oval; but in birds it is
often a long horizontal band, as in Figure 80a (minimizing the need for
eye movements) and has in it a central circular or oval fovea. In a num-
ber of birds a second fovea, seldom as well-developed as the central one,
lies temporally from the latter (Fig. 80b). Such a temporal fovea is
comparable with the single fovea of Dryopbis or a teleost, in that it and
its mate in the other eye can both be brought to bear upon the same
point in space ahead of the bird. The central or nasal fovea is useful
only for monocular vision sidewise from the head; and in most birds,
whose eyes aim much more sidewise than forward, it is the only fovea.
In the owls, only a fovea temporalis is ever present, and it may be very

Fig. 80 — Ophthalmoscopic appearance of bird eyes, showing pecten (ventrally),
arecE, and fovea. After Wood.

a, right eye of pigeon guillemot, Cepphus columba, showing horizontal linear area centralis
and single central fovea, x 3. b, right eye of Anna's hummingbird, Calypte anna, showing
central foveate area, and temporal fovea (in cutaway; cf. Figs. 114-5, pp. 308-9). x 10.

shallow or even lacking. One swift, Apiis apus, approaches the owls
in that its central fovea is barely visible though the temporal one is
well developed. Only birds ever have two foveae per eye, but George
Moore has recently found that some of the killifishes {Fundulus spp.)
have two horizontal, ventro-temporal, ridge-like areae.

In diurnal birds and in most lizards, excepting the monitors and the
more chunky and sluggish of the skinks, the fovea is deep and its slope
Cclivus') is convex. This convexiclivate type of fovea (Fig. 81) occurs
only in the very best-constructed of areae centrales. The less perfect areae
of fishes, Sphenodon, owls, domestic birds, and man all have shallow
and concave Cconcaviclivate') foveae (Figs. 75b, 82). It is safe to say
that most of these (the fishes excepted) are degenerate and formerly,

ARE^ CENTRALES AND FOVEJE

189

in some ancestor, tended more toward the convexiclivate type of profile.
The visual cells of Sphenodon show that this animal was once diurnal
(see Chapter 16, section C) and at that time it no doubt had a fovea

Fig. 81 — Central (nasal) fovea of the European bank swallow.

Exemplifying the deep, convexiclivate type characteristic of birds and lizards. After Rochon-
Duvigneaud.

Fig. 82 — Fovea and surroundings in Sphenodon. x 90.

Illustrating the shallow, concaviciivate type characteristic of fishes and of those vertebrates
whose fovece have become degraded through domestication or the abandonment of strict
diurnality. s, sclera; c, chorioid; r, retina. (The retinal and chorioidal pigment have been
bleached from the section; note that only rods are present — this is the only rod fovea in a
terrestrial vertebrate).

190 ADAPTATIONS TO DIURNAL ACTIVITY

as acutely deep as that of any lizard. Its pure-rod retina was once a pure-
cone one, so that Sphenodon, having retained the fovea despite the trans-
mutation of its cones into rods, now enjoys the only pure-rod fovea
which is known to us, except for the very mysterious case of a reputed
fovea in one deep-sea fish (Bathytroctes). Similarly, the foveae were cer-
tainly much better developed in some of the owls' diurnal ancestors.
The shallowness and variability of the pigeon's fovea has long been con-
sidered the consequence of semi-domestication, for in the fully domesti-
cated fowls the fovea is gone completely. On the other hand, the con-
caviclivate foveae of the few foveate teleosts, and that of the only known
foveate turtle (Amy da) have probably never been any deeper — they seem
merely intended to counteract the convexity of the area centralis. And,
by the way, some pure-cone animals with extremely good vision — the
ground-squirrels, particularly — have never produced a fovea simply be-
cause their entire retina is built as well for acuity as is the macula of man.

If the variable, shallow, and gradually-curved human fovea has not
degenerated from a deeper and much more abrupt depression, it is diffi-
cult to see what could have called it into being. Its magnifying action on
the image is probably negligible compared with that of a convexiclivate
fovea. Nothing much seemis to be known as to the shape of the foveal
depression in some of the monkeys and apes which are more strongly
diurnal than man himself. In the marmoset (Hapale jacchus) however,
the fovea has a very steep clivus and a small flat floor. The sooty manga-
bey (Cercocebus torquatus) probably has the most cone-rich retina of
any primate, and its foveal cones are the longest and slenderest in mam-
mals; but the shape of its fovea is unfortunately in dispute. One or two
divisions of mankind — the Hottentots, certain natives of India, and the
Tierra del Fuegans — are known to have phenomenal visual acuity; but
the profiles of their foveae are not accurately known. Their sharpness of
sight has always been attributed to an unusual slenderness of the foveal
cones.

The distribution of areae and foveae, and particularly their topograph-
ical locations in various retinae, are discussed further in section C of
Chapter 10. As we have seen, the modifications themselves are devoted
entirely to the raising of local visual acuity, but their locations are of
such importance in connection with eye movements and space-perception
that their full significance can be gathered only from a later consider-
ation of these matters.

INTRA-OCULAR COLOR-FILTERS 191

(D) Intra-Ocular Color-Filters

Color vision itself is a potent aid to visual acuity in its broad sense,
and was certainly evolved for this application rather than for the
aesthetic ones which it has come to have in human vision. But color
vision is such a large topic, with so many ramifications, that it needs a
long section to itself (Chapter 12). In the present section, we shall con-
sider a group of devices which occur only in the eyes of diurnal animals
(some, not all, of which have color vision) and promote their visual
acuity, and which look at first glance as though they must have some-
thing to do with creating color vision — though actually they are just
as effective whether their owners happen to be able to distinguish hues
or not.

Types and Distribution — The yellow pigmentation of the human
area centralis — making it a macula lutea — was discovered by Soemmer-
ing in 1818, In 1840, Hannover first described the oil-droplets which are
characteristic of so many vertebrate cones (Fig. 22, p. 54). Some or all
of these are always yellow, when any pigment is present in them at all.
By 1867, Max Schultze had called attention to the fact that the rich
network of capillaries in the inner layers of the mammalian retina con-
stitutes an effective yellow screen through which the visual cells must
look. In 1887 Schiefferdecker found that in certain fishes the cornea is
yellow. (Soemmering, long years before, had seen the color in the pike,
but thought it to be in the aqueous humor) . Other species have recently
been added to Schiefferdecker's list, and in the past few years it has
been found that diurnal squirrels, tree-shrews, snakes, geckoes, and lam-
preys (except Geotrid) have yellow lenses. It has been known for many
years that the adult human lens is yellow, but not until very recently
has it transpired that this is actually of advantage to sharp vision in
bright light.

This imposing list of intra-ocular color-filters exhibits at first glance
considerable variety; but (see Table IV, pp. 200-1) they are almost all
yellow; and where they are not, they are still of long- wave colors — and
they are confined to diurnal vertebrates. It thus appears logical that some
inclusive interpretation may hold for all of them, and after a large num-
ber of false starts such an interpretation has finally been given. But until
a few years ago the macular pigment, retinal capillaries, and yellow comeae
were neglected or forgotten, and the yellow lenses went undiscovered for
a most surprisingly long time, while attention was fastened upon the

192 ADAPTATIONS TO DIURNAL ACTIVITY

colored oil-droplets. As long as these held the stage, the mental myopia
of investigators prevented anyone's noticing the other types of filters
and using them to help explain the baffling oil-droplets.

The Color-Vision Theory — The oil-droplets were formerly believed
to occur in a much greater variety of colors than is actually ever the case.
Those of birds seemingly ran the gamut of the visible spectrum; but
under modern apochromatic microscope lenses the violet, blue, and green
droplets lose their colors and are seen to be actually devoid of pigment.
They owe their chromatic appearance, under cruder lenses, to purely
optical phenomena. Only red, orange, and yellow droplets occur in birds
and turtles along with some colorless droplets. Most groups provided
with colored droplets contain nocturnal species whose droplets are all
colorless. The pigments involved are carotenoids, and those extractible
from chicken retinas have recently been tentatively identified as astacin,
sarcinene, and xanthophyll.

When belief was current in a more complete spectral representation,
the theory of oil-droplet function first advanced by Krause in 1863 (and
based at first upon the supposition that lizards, as well as birds, had 'all'
colors) was most popular, and still has adherents. According to this
theory, each color of oil-droplet makes possible the independent sen-
sation of the corresponding color in the spectrum. The supposition was
that the bird has but one (not three) photochemical substances in its
cone outer segments (see p. 91), and that this undifferentiated sub-
stance would be affected equally by any and all visible wavelengths of
light. Discrimination of wavelengths on a qualitative basis — color vision,
in other words — would be possible only if certain cones were allowed
to be stimulated only by certain wavelengths, others by other wave-
lengths, and so on. The differently colored oil-droplets, standing in the
pathway of the light on its course toward the percipient outer segments,
were supposed to ensure this differential stimulation of different sets of
cones, which in turn connected with different sets of brain cells in which
the respective color sensations were registered. This mechanism of color
vision has seemed so simple and plausible that some students of human
visual physiology have fled to it as a refuge from the necessity of think-
ing through the state of affairs where, as in man, color-vision occurs with
all the cones alike, and have postulated that minute colored oil-droplets
occur in human cones— the while being careful not to look to see if they
are really there.

COLOR-VISION THEORY OF OIL-DROPLETS 193

The ingenious color-vision theory of oil-droplet function falls to earth
under several blows: the number of oil-droplet colors does not in fact
correspond to the range of the bird's spectrum, which is now known to
be co-extensive or even a little wider than our own. Lizards have a com-
plete color-vision system, yet have only yellow oil-droplets. There are
vertebrates far below the birds — the fishes — that have color vision with-
out benefit of oil-droplets, which could then scarcely be considered a
primitive device for hue-discrimination. Most important of all, it has
been known (though almost forgotten) for decades that the cones of
the bird fovea contain only yellow droplets, the red ones stopping at
the margin of that all-important retinal pit. This demonstrates not only
how wholly illogical it is to suppose that the bird would be able to per-
ceive only yellow in the fovea, and all other colors only outside it, but
also that the different colors of droplets are of unequal importance and
have different uses, not one common function. The exclusively yellow
droplets in the avian fovea line up with the yellow filters, whether com-
posed of oil-droplets or not, of all other vertebrates. Yellow droplets
appeared first in evolution, in lower vertebrates; and where the oil-drop-
lets are decadent, as in nocturnal birds, some yellow ones may persist
but no red ones ever occur. The red filters of birds and turtles can be
temporarily ignored while we consider what the much more common
yellow filter may do for photopic vision.

Yellow Filters and Chromatic Aberration — The image formed by
the natural dioptric system of the eye does not lie in a single plane or
spherical surface, even when the object is a plane or a curved surface
concentric with the eye. The image has thickness, owing to aberration
which is of two kinds, spherical and chromatic. Spherical aberration
results from the failure of the cornea and lens to bring parallel rays to
a single point, and since it is chiefly caused by the improperly curved
peripheral portions of the corneal and lens surfaces, it is effectively
combatted by the pupil which acts as a 'stop'. When the refractive power
of the lens is increased in accommodation, the pupillary aperture auto-
matically contracts to afford the smaller stop which is then demanded.
Chromatic aberration is due to the fact that the different wavelengths
of white light are not all bent to the same extent when they are refracted
at boundary surfaces. The refractive index of a substance is thus differ-
ent for each wavelength — it is this phenomenon of 'dispersion' which
makes it possible for a prism to form a spectrum by sorting the 'colors'

194 ADAPTATIONS TO DIURNAL ACTIVITY

out of 'white' light. The shorter waves are bent most, longer waves pro-
gressively less. As Figure 29c (p. 82) shows, this results in a series of
focal points beyond a lens, the violet focus being nearest and the red
focus farthest away. The distance occupied by these foci is called the
linear chromatic aberration, and in the human eye it is considerably
more than the whole thickness of the retina. In the refractionist's lan-
guage, the aberration amounts to about two diopters. The 'normal' or

C

/

550

Wavelength (mp)

.401- m
t <

0 Q

Fig. 83 — Graph showing how yellow filters combat chromatic aberration.

(Curve of transmission spertrum smoothed from data of Ludvigh and McCarthy on absorp-
tion in the lens, cornea, and humors of the human eye, integrated with data of M. Sachs
on absorption in the most completely studied macula among his nine examples; dispersion
curve for the human dioptric media, showing the relative refrangibility of the various wave-
lengths, plotted from data of Polack).

The curves bring out the fact that the short waves, which are most strongly dispersed and
which consequently contribute most to chromatic aberration (c/. Fig. 29c, p. 82), are the
ones most strongly absorbed (i.e., least well transmitted) by the yellow filters interposed
in their path within the eye.

emmetropic human eye is actually emmetropic only for yellow light, and
is, simultaneously, 0.75 diopters hypermetropic for red and 1.25 diopters
myopic for violet. Since the dioptric apparatus ordinarily places the
yellow focus in the visual-cell layer, we must actually accommodate when
diverting our attention from a blue object to a red one at the same
actual distance from the eye, and must relax accommodation upon look-
ing back at the blue object. This fact is employed by astute artists to
heighten the illusion of depth in their paintings.

YELLOW FILTERS AND CHROMATIC ABERRATION 195

If a particular color-focus lies squarely in the visual-cell layer, the ho-
monomous color-value of the external visual field will be crisply focused
but all others will be represented, at the level of the visual cells, by sets
of blur-circles. Fortunately the ends of the spectrum are much less bright
than the yellow region; but even so, chromatic aberration results in a
considerable blurring of the image.

In the fovea, chromatic aberration is partly compensated for (except in
birds) , by the greater length of the foveal cones (how many things we
find we can do with that greater length!), for a greater number of color-
foci can thus lie in the length of one cone. But foveal cones have their
limits in length, and fall far short of dealing adequately with chromatic
aberration by such means. Obviously, there would be no chromatic aber-
ration if a single wavelength of light were passing through the eye to the
receptor layer. To bring this about, however, would mean the elimination
of color vision — and of nearly all the light. A compromise must, then, be
made by which the spectrum is narrowed down enough to make a big
dent in chromatic aberration, without sacrificing much of the physiologi-
cally effective energy of whole sunlight, or many of the colors which
occur most commonly in nature.

A yellow filter serves this purpose admirably. It cuts out much of the
violet light and some of the blue, which are the colors responsible for
most of the chromatic aberration, as Figure 83 demonstrates. At the same
time it lets through, unimpeded, most of nature's hues, and passes the
spectral regions which look brightest to both light- and dark-adapted eyes.

Other Values — This reduction of the effects of chromatic aberration is
not the only performance of a yellow filter. Most scattered light is of
short wavelengths, and under bright-light conditions this scattered light
results in glare. Glare and dazzle are minimized by a yellow falter. Simi-
larly, the unfocusable shortwave light scattered in the atmosphere, and
responsible for the bluish cast of distant mountains and for the blue of
the sky, is cut out by a yellow filter which, as every photographer knows^
creates a sharper image.

Still another effect is the enhancement of contrast. It will be recalled
that the same color-sensation can be aroused by different mixtures of
wavelengths. One can easily find, say, two books on the shelf whose col-
ors appear to be identical blues or greens. Yet a spectral analysis of the
light reflected from them might show the like-seeming colors to be wholly
different in wavelength composition. Almost any filter of colored glass or

196 ADAPTATIONS TO DIURNAL ACTIVITY

gelatine, placed before the eye, will make the two books look unlike; for
certain wavelengths reflected by the pigment of one, and absorbed by the
filter so as to change the color seen through the latter, are not necessarily
emanating from the other pigment at all. By absorbing wavelengths com-
mon to the two unlike mixtures, the filter brings out the fact that they
are unlike, which is something the unaided eye cannot detect.

A filter thus produces contrast between colored areas which otherwise
would look alike and would therefore be without a discernible boundary
between them. This fact was put to important use in World War I, when
colored goggles worn by reconnaissance aviators enabled them to detect
green camouflage produced by paints whose reflection-spectra were not at
all like those of the chlorophylls of actual foliage. Modern 'foliage'
camouflaging is more troublesome to both adversaries, for it has to con-
sist of actual foliage, which must be replaced frequently as it fades.

A filter naturally tends to abolish just as many contrasts as it pro-
motes; but promotion is in advance of abolition when yellow filters
and natural colors are under consideration. By cutting out the different
amounts of blue in different but alike-looking green mixtures, the greens
are made to look unlike; and almost any other contrasts can be sacrificed
by the animal if only those between greens, so numerous in nature, can be
enhanced. The oil-droplet type of filter has a special advantage, since the
many colorless or other-colored droplets scattered among the yellow ones
in the whole mosaic will permit the perception of any contrasts which the
yellow droplets tend to iron out, and vice versa. By altering the propor-
tions of the different colors of droplets in different parts of the retina,
particular color-contrasts are enhanced in particular parts of the visual
field. Thus in the pigeon the ventronasal three-quarters of the retina have
the yellow droplets predominant, giving maximal contrast of objects seen
against the sky by eliminating the latter's blue color; while the dorso-
temporal quadrant, being especially rich in red droplets, affords maximal
visibility to objects seen against the green of the fields and trees over
which the bird is flying. In World War II, antiaircraft observers have
stumbled onto such tricks, and have learned to use filters when scanning
the sky for enemy planes.

One thing which yellow filters might do— but don't— would be to absorb
harmful ultra-violet rays before these could reach the delicate cone outer
segments. Experiments have shown, however, that none of these rays sur-
vive absorption in the cornea and lens of a pigeon's eye, whose oil-drop-
lets consequently cannot possibly be purposed to protect against them.

OTHER VALUES OF YELLOW AND RED FILTERS 197

Red Filters and the Rayleigh Effect — A very widespread supersti-
tion, showing itself in such things as red airport beacons and amber fog-
lights on automobiles, is the notion that some colors — notably red — pen-
etrate fog better than do other colors or white light. The supposed phe-
nomenon is attributed to the 'Rayleigh effect', which is the scattering of
light inversely as the fourth power of the wavelength. The short waves
are scattered the most, the red and infra-red ones scarcely at all, resulting
in the blue coloration of the sky and in the remarkable clear pictures
which can be taken through haze with infra-red-sensitive plates.

But as far as the visible spectrum is concerned, there is no Rayleigh
scattering at all when the particles which cause the scattering are larger
in diameter than 0.75 [X. Natural mist and fog droplets, and solid particles
suspended in natural waters, are invariably at least several times this size,
and scatter light quite irrespective of wavelength. Red oil-droplets can-
not, then, be designed to sharpen images by eliminating Rayleigh-scat-
tered light in misty weather or in water, as some have thought. The tur-
tles and birds have nothing in common, and if this inclusive explanation
will not hold for the red oil-droplets of the two groups, room is left for
independent explanations of the two cases.

Value of Red Oil-Droplets in Birds — Most birds are such early ris-
ers that they expose themselves to Rayleigh scattering — not by gross mist
particles, but by molecules of water and gases in the atmosphere of even
the clearest of sunrises. At this time of day the sun's rays slant through
such a long atmospheric pathway that they appear reddened, the same
being true of the sunset — which is more familiar to most of us. The bird,
getting in most of his day's work at dawn and shortly after, is aided by
his red droplets. As the day wears on and the sunlight whitens, the yellow
(and on dull days, the colorless) droplets take over — the orange ones
affording a smooth transition. If this explanation is true, one would ex-
pect late-rising birds to have few red droplets. This is indeed the case, for
whereas the song-birds average 20% red droplets, the hawks have but half
of this number; and in the crepuscular swifts and swallows there are but
3% to 5% red droplets.

Value of Red Oil-Droplets in Turtles — The significance of the red
droplets of turtles is rather different. More than any other diurnal verte-
brates, they have the problem of seeing over the glary surface of water.
Since they have intensity to spare, they can afford red droplets for the
even greater effect upon chromatic aberration which a red filter will have,

198 ADAPTATIONS TO DIURNAL ACTIVITY

as compared with a compromise yellow one. On less bright days, the tur-
tle's yellow, or even his colorless, droplets automatically replace the red
ones as the most important constituents of the whole mosiac. Thus the
birds and turtles, having sufficiently cone-rich retinae, have been able to
differentiate the cones into several populations. Where most retinae are
rod-and-cone, or duplex, the turtles and birds have produced what may
fairly be called multiplex vision.

The workings of the turtle's oil-droplet mosaic can best be gathered
from an account of a clumsy, man-made imitation worked out empirically
by the United States Navy, as described to the author by Mr. Laurence
Radford of the Bureau of Ordnance :

"The Navy uses both red and yellow color filters in optical instru-
ments. Both are made of Corning Glass. The red cuts quite sharply at
about ^6000-6200 [A.u.j and the yellow at about ?u5 100-5300 [A.u.].
These filters are used because much experience has shown that they are
helpful, and the particular filters selected were chosen after considerable
study, both experimental and theoretical.

"In my opinion these filters are effective for our purposes because they
reduce glare due to scattered light and minimize the eflFects of the chro-
matic aberration of the eye, and for these reasons almost exclusively.
These two effects are produced more intensively by red than by yellow
filters, i. e., the amount of scattered light transmitted by the red is much
less than by the yellow because the latter transmits the green; and with
the red filter the effect of chromatic aberration is practically eliminated.
But there are conditions when the red filter cannot be used effectively,
perhaps because of insufficient intensity of illumination, or perhaps be-
cause it would reduce the color contrast. Hence the two colors, giving us
essentially the choice of two degrees of the same effect."

The red and yellow oil-droplets of the domestic hen have been found
to cut the spectrum off respectively at ^5800-5900 A.u. and ^5150-5250
A.U., the extracted red pigment (astacin) and yellow pigment (xantho-
phyll) at A,5900A.u. and ^5200 A.u. respectively when dissolved in
castor oil. Perhaps when the droplets of turtles are studied more carefully
they will be found to come even closer to justifying the Navy's choices!

In this connection it is significant that the kingfisher, whose visual
problem, like that of the turtle, is complicated by glary water, has 60%
red droplets — three times as many as the average bird. So much for the
functions of the intra-ocular color-filters. Some remarks on their nature
and evolution are now in order.

PHYLOGENY, CHEMISTRY OF FILTERS 199

Phytogeny and Chemistry of the Intra-Ocular Filters — The old-
est of all appears to be the yellow lens, which occurs in lampreys (but
not in the nocturnal Geotria) . Here, as well as in snakes and squirrels,
the pigment involved (lentiflavin) is soluble in weak alkalies. It is pres-
ent in full amount in albino squirrels, hence cannot be scattered melanin,
but is a chemically distinct substance (consult Table IV, next page).

In at least one of the two or three diurnal geckoes (Lygodactylus) , and
in the strongly diurnal, squirrel-like tree-shrews (Tupaia) the lens is also
yellow though nothing is as yet known about the pigment itself. Presum-
ably it is lentiflavin which, since it has been evolved repeatedly in such
widely-scattered groups, probably has as its precursor some substance
which is present in all vertebrate lenses.

The most intense colorations of the lens are reached in the ground-
squirrels and prairie-dogs, where the lens is almost orange. The lenses of
all other American sciurids (excepting the pale ones of the gray squirrel
and the colorless ones of the flying squirrels) are alike in color and are
matched by a 2 mm. thickness of American Optical Company 'Noviol 0'
glass. 'Noviol 0' is matched by the lens of Malpolon monspessulanis,
regarded as the most sharp-sighted snake in Europe, and will probably be
found to be exceeded in coloration by the lenses of Dryophis and its rela-
tives. Other diurnal snakes have paler lenses, the coloration being deep-
est in swift, bright-light species such as the racers and whipsnakes. Cre-
puscular snakes have little lentiflavin, nocturnal species none at all. Lam-
prey, Lygodactylus, and Tupaia lenses compare with those of a gray
squirrel or a whipsnake.

The yellow coloration of the human lens is the result of a precocious
aging of the lens nucleus which commences actually before birth, and is
thus not on the same footing as that of other yellow lenses. It grows
steadily in depth throughout life — the lens of a child has been found to
absorb 10% of the blue light entering the eye, that of a 78-year-old man
85%. In the normal adult human eye, absorption in the dioptric media
increases gradually from the long-wave to the short-wave end of the spec-
trum, attaining a value of over 90% in the violet. In old age the spec-
trum is cut off in the blue-green region and aged artists find that their
blue-containing pigment mixtures look wrong to younger persons, unless
the painting is done under an illumination which is particularly rich in
short-wave light, such as that from a mercury vapor lamp. The pigment
is melanin formed by the interaction of protamine and cysteine liberated
by protein-breakdown. The development of the coloration is thus due to

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202 ADAPTATIONS TO DIURNAL ACTIVITY

an essentially senescent change, and its optical usefulness is the sheerest
of accidents.

Oil-droplets and yellow corneae both appear first in the chondrostean
and holostean fishes respectively. The oil-droplets of the sturgeon are
colorless, though they were not necessarily always so. They have been
used as an argument that the oil-droplet was first evolved as a colorless
focusing device; but the sturgeon has a nocturnally-adapted eye, and one
would expect its oil-droplets to be colorless even if they had been pig-
mented in some diurnal ancestor.

In the diurnal Amia, the whole cornea is yellow, with the color intensi-
fied dorsally. The pigment itself has not been studied, but it is probably
the same ichthyocarotin which occurs in many of the dermal chromato-
phores of fishes generally. Some teleosts, notably the markedly diurnal
pikes (Esox spp.) have as strongly yellowed corneae as Amia. In a spe-
cies of darter from Georgia, so new to science that as yet it has no name,
Hubbs reports a central, homogeneous, deep yellow coloration in the
cornea, opposite to and co-extensive with the pupil. Other teleosts have
various, usually diffuse and pallid yellow colorations; but in most species
the cornea is quite colorless. However much a fish may prefer bright sun-
light, that light is dimmer through water than it would be on land. No
fish can see more than a few rods at best owing to the extinction of
light in water, hence few can afford the luxury of a yellow filter unless
they are content to use their eyes mostly near the surface. Most fishes
enter deep, dim water at some time of the year. They must also do with-
out vision when beneath a covering of ice and snow. The eels are
exceptional, below the mammals, in having retinal capillaries; but these
are not intended as a filter — their significance is a very special one (see
pp. 405-6).

Of the amphibians, only the frogs approach diurnality, and these have
oil-droplets which may be colorless, or yellowed by the same carotenoid
pigment which colors the animal's fat. Other amphibians lack even color-
less droplets.

Among the reptiles Sphenodon is at once conspicuous since, though
nocturnal, and with its visual cells almost all converted from cones into
massive rods (see Chapter 16, section C), the oil-droplets and some yel-
low pigmentation thereof have been retained. The reader will remember
that Sphenodon has also kept the fovea of its diurnal forebears. (Fig.
82, p. 189). The turtles have ruby-red, orange, and lemon-yellow oil-
droplets. The crocodilians, like the similarly nocturnal toads, have got-

PHYLOGENY, CHEMISTRY OF FILTERS 203

ten rid of all droplets. So have many lizards and the snakes; and it is
in these two groups that we find evidence that once the oil-droplets have
been lost, they can never be regained :

Most lizards are diurnal and have bright yellow and colorless oil-drop-
lets. In the chameleons, there is claimed to be an additional yellow pig-
mentation of the inner layers of the retina in the region of the fovea,
though this matter requires further investigation. Secretive and fossorial
lizards such as Anniella have lost most of the pigment of the oil-drop-
lets, and nocturnal above-ground forms like Xantusia and Heloderma
have only completely colorless droplets. The logical final step has been
taken by the geckoes, which probably passed through a Xantusia-Vkt
stage (consult Fig. 25, p. 62) but later eliminated the useless, color-
less oil-droplet entirely. Some geckoes are so small, with such tiny eyes
(e. g., Sphcerodactylus and Gonatodes spp.), that they are able to be
more or less diurnal without benefit of a slit pupil. A couple of genera of
good-sized geckoes {Phelsuma and Lygodactylus) are round-pupilled
and diurnal, and have eyes large enough to demand special provisions for
this habit. It is probable that in them the visual cells have been recon-
verted into cones, and in Lygodactylus at least the lens is known to be
yellow.

The bearing of the structure of the eye upon the problem of the origin
of the snakes will be discussed later (Chapter 16, section D) ; suffice it to
say here that their lack of oil-droplets shows them to have originated as
light-shunning forms. The yellow lens has appeared here (as in Lygo-
dactylus and the squirrels) because the oil-droplets could not reappear,
upon the adoption of diurnality by forms whose photophobic ancestors
had discarded them. It is safe to say that any group which has oil-drop-
lets has had unbroken ancestry in forms similarly provided. Thus, the
presence of yellow droplets in frogs indicates that the early amphibians,
the Stegocephali, had droplets and were diurnal— as indeed we should
surmise from their bulk, their consequent need of the warmth of the sun,
and their complete freedom from terrestrial enemies during their evolu-
tion from the fishes. A similar argument would attribute diurnality to
the dinosaurian ancestors of the birds.

Of the mammals, the monotremes are usually called nocturnal though
the duck-bill is not strictly so, and has oil-droplets whose color or lack of
it has not been ascertained. Droplets occur in marsupials but are always
colorless so far as is known, though once erroneously reported to be pig-
mented in kangaroos. The placental mammals are nearly all crepuscular

204 ADAPTATIONS TO DIURNAL ACTIVITY

or nocturnal, with twenty-four-hour eyes among the ungulates and car-
nivores. None of these have filters. Only a few placental mammals,
mostly squirrels or primates, are strongly diurnal. The yellow lenses of
tree-shrews and squirrels, like those of diurnal geckoes and snakes, are to
be looked upon as substitutes for the irretrievable oil-droplets of remote
diurnal ancestors, which had been discarded by more immediate noc-
turnal ancestors.

The retinal capillary supply likewise makes its first appearance (except
for the eels) among the mammals, and cannot be ignored as a yellow-
filtering device. However, it is the least effective of all such devices, for
the capillaries are in general no less abundant in nocturnal mammals
than in diurnal ones, indicating that they absorb so little light that they
do not interfere with scotopic vision. Again, in areas centrales the capil-
lary network is not richer but is actually diminished, as though the shad-
ows of the vessels caused damage to the image which was not compen-
sated for by any differential filtering action. In the few mammalian areae
which have foveal depressions the capillaries are eliminated entirely. It is
in such areae (in the primates) that we find yellow pigment in the inner
layers of the retina — filling in, as it were, the lacuna in the capillary
plexus, but far more efficient as a filter than any equal area of the capil-
lary screen.

The nature of this pigment in the macula lutea is unknown. No studies
have been made of its status in sub-human primates. The amount is
known to vary greatly in different human individuals — being sometimes
so great as to render the person wholly blind to blue. Old observations,
now considered questionable, seemed to demonstrate more of the pig-
ment in brown-eyed than in blue-eyed persons. It has been claimed to be
soluble in alcohol and to change color in acids and alkalies. No modern
biochemist has given any attention to the pigment or to a resolution of
these apparent ambiguities of genetic and chemical behavior; but a fair
guess is that the substance belongs to the carotenoid family of pigments
and may be subject to the influence of diet. Simple experiments on the
perceptibility of blue stimuli would show whether the macular pigment
can be increased by feeding carotene or related substances to human
subjects; but such experiments have yet to be made.

The effectiveness, in human vision, of the combination of macular
pigment and the yellow lens is difficult to evaluate. We do know that
for a few weeks after a person has had cataracts removed, white light
looks decidedly bluish to him. We can only guess how much less sharply

PHYLOGENY, CHEMISTRY OF FILTERS 205

we would see without our filters, by determining how much more sharply
we see with additional yellow filters placed outside the eye. The fact that
we can gain appreciably in visual acuity by that means — as any expert
rifleman knows — shows, by analogy with the squirrel species of various
brightness-preferences, that the human eye is not purposed for use in
the very brightest of light. The prairie-dog, which prefers such light,
has his intra-ocular filter already so deeply colored that any extra-ocular
supplement to it would probably take more away from his vision than
it conferred. We are also led to consider man as not inherently strictly
diurnal by the fact that the ground-squirrel, the bird, or the diurnal
reptile unblinkingly tolerates intensities which force us to screw up our
eyelids or run for a pair of dark goggles.

Chapter 9
ADAPTATIONS TO NOCTURNAL ACTIVITY

(A) NOCTURNALITY AND THE EyE

Nocturnality and Crude Vision — The support of nocturnality, in
animals whose eyes mean much to them, comes wholly from great sensi-
tivity to light. This is possible only with a preponderance of rods in the
retina, which in turn makes for low visual acuity. However, if a noc-
turnal animal emphasizes rhodopsin and the length of his rods rather
than their diameters, and keeps summation in optic nerve fibers at a
minimum, he may be able to retain good resolving power in bright light
— ^provided he has means of reducing greatly the sensitivity of the eye
under those conditions. Such means, as we shall see, are exemplified by
the common slit-shaped pupil and the rare occlusible version of the
'tapetum lucidum'; and the geckoes show what can be done to make an
extremely sensitive eye very valuable in the daytime even to an essen-
tially nocturnal animal, if that animal insists upon being able to come
out by day with safety.

Nocturnal adaptation of the eye need not, therefore, be as restrictive
as bright-light adaptation. No cone-rich or pure-cone eye is useful at
night, but a pure-rod eye may be quite useful by day. But it is only
among the geckoes, in Sphenodon, and perhaps in the owls that forms
having great sensitivity have been able to combine with it a respectable
degree of resolving power. By and large, ocular adaptations for sensi-
tivity demand such a sacrifice of visual acuity that they make nocturnal
animals largely dependent upon senses other than vision.

The nocturnal animal is primarily an ear- and nose-animal; and this
is particularly true of aquatic forms, to which the chemical and auditory
senses are especially important because of their enhanced value over
distances in water. Both audition and olfaction are promoted under
nocturnal conditions, though not because of anything the nocturnal
animal has done to modify the receptors of those senses. Odors and
sounds are carried better by the night air and are dispelled more slowly
because of the absence of rising air-currents. At night, too, sounds have
an augmented attention-value since they are of fewer kinds and are out
of competition with abundant visual stimuli.

NOCTURNALITY AND VISUAL ACUITY 207

The diurnal animal, because he is cone-rich, has an acuity of vision
which makes the eye his best sensory instrument; but the nocturnal form,
being cone-poor, has unsharp vision and can make more accurate identi-
fications of enemies and food with his nose than with his eyes. The
'minimum separabile for parallel lines — the angular distance they must
be apart to be seen as separate — has been determined experimentally for
a number of animals by various investigators. Some of the values ob-
tained, not necessarily at all close to maximal and minimal values for all
vertebrates, are listed in Table V.

Table V

VISUAL ACUITIES FOR PARALLEL LINES (From various sources)

, . , Visual Corresponding distance Visual angle corresponding

Diurnal animals: angle, on retina, to imm. distance

minutes micra along visual cortex

Human adult 0.44 L89

0.48 2.06

0.50 2.14

(different reports) 0.80 3.43

0.82 3.52

0.83 3.56

Child 0.62 2.67

Chimpanzee 0.47 1.86

Rhesus monkey 0.67 2.33

Rhesus monkey,

along visual axis 4'

Rhesus monkey,

7° from visual axis 20'

Cebus monkey 0.95 3.31

Pigeon 2.70 4.89

Pigeon, 'homer' 0.38 .69

Gamecock (no fovea) 4.07 9.58

Nocturnal animals:

Cat, along visual axis 5.5 1°

Cat, 30° below axis 5°

Alligator 11.0

Opossum 11.0

Rat, pigmented 26.0 23.8

Rat, albino 52.0 47.7

208 ADAPTATIONS TO NOCTURNAL ACTIVITY

Advantages and Limitations — It may be stated categorically that
nocturnality, wherever it is characteristic of a large taxomic group, has
always been adopted secondarily by the ancestral form of the group.
Even more certainly, any nocturnal member of an otherwise diurnal
group has become nocturnal independently. We can be sure that all
vertebrate species would be diurnal if they could 'get away with it'.

The original chordates were bright-light animals. The early fishes
invented rods in order to extend their day and to be able to venture
from the surface to depths where they were safer, but where the lessened
illumination made necessary greater ocular sensitivity. The first land
animals were quite without predaceous enemies and were able to enjoy
the benefits of sunshine by becoming diurnal and heliothermic. But
increasing competition on land drove some forms into the cavern of
nocturnality to escape their enemies and to be able to feed in compara-
tive peace. These nocturnal amphibians and reptiles were the better off,
the smaller their bodies and the less they were dependent upon the sun
for the maintenance of rapid metabolism. The advent of small-bodied
descendants of the massive stegocephalians made nocturnality desirable
for the reduction of water-loss; and the small animal, being able to be
more active at a given environmental temperature, suffered no disad-
vantage from the change in habits.

Upon the invention of 'warm-bloodedness', independence of the sun
became greater. The mammals for the most part proceeded to become
crepuscular and nocturnal. The defenseless plant-eaters then found
greater safety in feeding, which is in them an almost continuous and
decidedly noisy process which places the animal at a real auditory dis-
advantage. Predators were forced into nocturnality by the paucity of
diurnal prey. The birds, however, were mostly prevented from aban-
doning diurnality by the high requirements imposed upon visual acuity
by the habit of flight. The ability to fly, in itself, served as a compensa-
tory defense against most predators, for birds are most vulnerable in the
form of eggs and young, as easily captured at one time of day as another.
The most conspicuously nocturnal birds, the owls, trace their ancestry
from diurnal birds through the crepuscular goat-suckers and frog-mouths.
They had no trouble in becoming nocturnal, for with their size and
roundheadedness, there was abundance of room in their heads for eyes
large enough to combine fair resolution with super-sensitivity.

Though nocturnality is something of a sanctuary from predators and
carries with it a coincidental improvement of audition and olfaction

ADVANTAGES, LIMITATIONS; LIGHTLESS HABITATS 209

(available also, of course, to the nocturnal predator) it imposes some
restrictions on diet. Tiny food objects cannot so easily be discerned, and
we find nocturnal animals to be relatively gross feeders, cropping vege-
tation which they have located by scent, rather than pecking at seeds,
and seizing large, unaware prey or motionless nestlings rather than
running down minute insects. Where insects do constitute the food, they
are not usually caught individually after visual location, but are 'trawled'
in numbers, as by the sticky tongue of an ant-eater. Seeds are sought in
numbers also— the rodents proverbially prefer their seeds in bunches,
as in a head of wheat or an ear of maize.

The superior visual acuity of the diurnal vertebrate often enables him
to maintain an enormous disparity between his armament and the de-
fenses of his prey — as when a hawk seizes a garter-snake or a kingbird
catches a fly. The nocturnal carnivore must have superior weapons, for
he must usually fight on more nearly equal terms with relatively much
larger prey. He prefers to catch nocturnal prey at a disadvantage in the
daytime, and it is not surprising that carnivorous forms are as often
twenty-four-hour animals as strictly nocturnal ones. The very strictest
of nocturnality is seen among those preyed-upon animals which are so
defenseless that they dare not come out of their hidey-holes even to bask.
In this category fall most of the legions of rodents.

Lightless Habitats and their Conquest — At this point we should
give a moment's attention to the fact that in addition to nocturnality
Ijy the clock', there are several other dim-light habits of vertebrates
which might seem to call for the same ocular modifications : the fossorial
habit (as exhibited by the mole, as opposed to forms like the woodchuck
which live in a burrow but use it only as a home) ; the cave-dwelling
habit (as developed by the permanent residents of caves in contrast to
such animals as the bats, which use caves only temporarily; the intern-
ally-parasitic habit; the deep-sea habit; and the occupation of very mud-
dy waters.

The habitats involved here are practically or entirely lightless, and
the animals which have adopted them have, for the most part, given
up any attempt to see and have allowed the eye to degenerate to a tiny,
even microscopic vestige, or to vanish altogether (see also pp. 387-405,
and Fig. 133). Well-developed eyes, adapted for dim-light vision, are
found only in those forms which occasionally venture into one of these
habitats for purposes other than mere temporary concealment; and out-

210 ADAPTATIONS TO NOCTURNAL ACTIVITY

side of the vertically-wandering fishes and whales these are very few
indeed. There are many other exceptions constituted by the deep-sea
fishes, most of which have enormous eyes whose retention and perfection
we can safely attribute to the timely invention of light-producing organs
by deep-sea animals. There is some point to a retention of a sense of light
and darkness by subterranean forms so that they may be aware when
their burrows have been broken into by the weather or by other animals.
Such animals, like the moles, marsupial moles, Spalax, and the fossorial
reptiles always have enough of an eye to make this much Vision' possible.
But the strictly cavernicolous vertebrates, all of them fishes or salaman-
ders, have only microscopic, completely non-functional eyes. Of the two
dozen or more cave-dwelling species of fishes, only two or three ever (as
individual variations) exhibit useful eyes, and in only one of these (the
Mexican Anoptichthys jordani) do the eyes vary from zero to complete
normality. The same degree of degeneracy as in cave fishes is seen in the
parasitic hag-fishes, which 'burrow' — in the bodies of their prey!

As for the muddy-water problem: several kinds of gobies and at
least one mammal (the fresh-water dolphin Platanista gangetica, swim-
ming through the roiled waters of the great Indian rivers), have given
it up as an impossible job. The eye of Platanista has 'gone bad' in a
unique way — this is the only vertebrate with a macroscopic eye which
lacks all traces of a lens. In such limicolous gobies as Austrolethops and
Trypauchen, and in the sole Typhlachirus, the entire eye is minute or
quite obsolescent. In general, the fishes of silty rivers, as in our Great
Plains, have somewhat undersized eyes which are useful only close to
the surface, where alone there is adequate light. The fishes of the peculiar
Lake Balaton have however made a valiant effort to cling to vision
despite the quasi-opacity of the water in which they swim (see p. 236).

The Eye as a Whole — It was hinted earlier (p. 172) that nocturnal
animals, as well as diurnal ones, have a special need for a large eye. The
need is a very direct one in the case of a diurnal eye: to enlarge the
image. The reason why large eyes are desirable for a nocturnal animal is
a little more complicated. It is not at all for the improvement of resolving
power — a whale eye the size of a baseball has but 2% of the resolving
power of the human eye, due to its tremendous retinal summation.

If we could be watching an animal in the process of evolving nocturn-
ality, we might feel impelled to advise him to enlarge his eyes "so more
light can enter them." But on second thought we should realize that this

THE NOCTURNAL EYE 211

would only tend to dim the image on the retina. Doubling the diameter
of the eye will double the diameter of the retinal image. This will reduce
the illumination per unit area of that image to one-fourth. But suppose
the pupil enlarges in proportion to the whole eye. Doubling its diameter
will increase, by four times, the amount of light it admits. The illum-
ination of the retina will thus have the same strength in any and all
eyes whose proportions are exactly the same, regardless of their abso-
lute sizes.

An eye which is simply larger will not, then, have brighter images and
greater overall sensitivity in dim light. But enlarging the pupil more yet,
out of proportion to the size of the eye, will brighten the image. If the
pupil is enlarged the lens must be broadened too, if spherical aberration
is not to be increased. A broader iris (to make room for a larger pupil)
and a broader (and proportionately thicker) lens will, in themselves, call
for an increase in the absolute size of the eye if it is to remain mechan-
ically and biologically in balance. We have arrived, by a rather devious
route, at a justification for advising our nocturnally-inclined animal to
enlarge his eyes — and to enlarge them in a disharmonic manner.

Enlarging the lens 'out of proportion' to the eye moves the optical
center of the cornea-lens apparatus backward (Fig. 71, p. 173). When the
curvature of the cornea, lens, or both is now sharpened to keep the image
from receding behind the retina, we find that the anterior chamber has
deepened and the image has shrunk. This shrinkage of the image is fine
up to a certain point, for it accomplishes what was wished : that bright-
ening of the image which lets the eye operate in dimmer light. The retina
of such an animal being poor in cones, visual acuity is low enough in all
conscience already, but it may suffer too much unless now the eye is en-
larged harmonically still further, to spread the image without detracting
from its brightness. That species is fortunate which has head-room for
the development of sensitivity through eye size alone. The cat has a
large eye for its size, but a proportionately small retinal image — only
38% of the diameter of that of the horse, whereas the diameter of the
eyeball is 50% of that of the horse. The human ocular axis is only 1.19
times that of the cat, but man's retinal image is 1.37 times as broad as the
cat's. Some small, small-eyed animals have had to do the whole job by
making the lens spherical, the cornea perhaps remaining broadly curved
since the lens has more to do with pulling backward, into the eye, the
optical center whose distance from the retina determines the size of the
image. The large-eyed carnivores such as the cats have greatly sharpened

212 ADAPTATIONS TO NOCTURNAL ACTIVITY

the curvature of the cornea and thus have been able to keep the lens
from becoming so large and so round as to increase spherical aberration
to any disastrous extent.

The end result of the juggling of these factors is an eye which, as
compared with a diurnal eye such as that of man, is :

1. Relatively large for the size of the animal, and absolutely large if
there is room for it in the head — even altered in shape ('tubular' eyes —
v.i.) if there is not space enough for an orthodox eye.

2. Provided with a relatively large anterior segment, making room
for a large-opening pupil and a proportionately large lens, which is :

3. More nearly or even quite spherical and set far back from the
cornea (which where convenient is less sharply curved), so that the
anterior chamber is often deepened and:

4. The optical center is far back within the eye, resulting in a smaller
and brighter retinal image.

'Tubular' Eyes — There are certain interesting consequences of these
changes which, in themselves, add nothing to the capacity of the eye for
operation in dim light. Whereas the diurnal eye tends to have a small
anterior segment and a large fundus, the nocturnal eye tends to have a
large anterior segment and, the image being small, would gain nothing
from having a posterior segment proportioned to it as in a diurnal eye.
The result is a relatively small fundus, rendering the eye somewhat
tubular in some species in which the anterior segment has become enor-
mous. This is true of the owls and their relative Podargus, some lemu-
roids, and a majority of the deep-sea fishes which have kept their eyes.
These forms, so to say, have ballooned the eye to the point where there
is barely room for it in the head (Fig. 84), and have continued to en-
large the anterior segment so that the effect is produced of the useless
equatorial region of the globe having been cut away (Fig. 136b, p. 400).
The eye of the deep-sea fish bears the same relation to a standard-shaped
fish eye of the same axial length as does the part of an apple, removed
by a cylindrical coring tool, to the intact apple.

The small size of the retina in tubular nocturnal eyes tends to make
more narrow the angle which embraces the visual field outside of the
eye. This demands considerable rotability of the eyeball in the orbit, in
order that the animal shall be able to see about him through a safely
wide angle. But, these tubular eyes have become so large that they are

'TUBULAR' EYES; SPHERICAL LENSES 213

locked in a close-fitting orbit and cannot be turned. Even though the
oculomotor muscles are present in owls, the eye of an owl cannot be
moved in the orbit by force. In consequence, the owls and the lowest
primates (e.g., Tarsius) have evolved an extraordinary rotability of the
head upon the axis of the body. The neck in all birds is notoriously
flexible — even the strictly diurnal hawks can rotate the head about 180 ;
but the owls can revolve theirs through 270° or more. To explore their
surroundings visually, the deep-sea fishes, lacking a neck, must turn the
whole body, or bend the trunk if they are slim enough to do so.

Spherical Lenses — Where the eyes of small nocturnal animals have
remained spherical and not enlarged unreasonably, the lens is always
even larger in proportion than in tubular eyes. In fact, when the lens

Fig. 84 — Tubular (miscalled 'telescopic' ) eyes.

a, owl, Bubo sp. x 1. After Putter, b, prosimian, Galago crassicaudatus garnetti. x2.46.
After Franz, c, deep-sea fish, Argyropelecus sp. Redrawn from Hesse.

swells (through evolution) in size it swells also in shape, so to say, and
tends toward a sphere (Fig. 71, p. 173). When it has attained this shape,
as in small bats, most rodents, and the rodent-like opossums, an advan-
tage is gained in connection with the need for voluntary eye movements
— the latter can be allowed to diminish or even to disappear. Part of the
reason for this is the absence of an area centralis, owing either to its dis-
appearance or to a failure to evolve one. Since there is no reason to aim
any particular retinal spot at the object under scrutiny, there is no reason
for aiming the eye at all. Largely, however, the diminution of eye move-
ment is due to the periscopic action of a spherical lens when associated
with a concentric or nearly concentric retina. Such a lens casts an image
which is small, but is equally good from whatever direction the object

214 ADAPTATIONS TO NOCTURNAL ACTIVITY

is imaged. Hence the eye with a spherical lens sees its object about as
well in the periphery of the retina as in the fundus. A moving object can
therefore travel farther alongside or around the head of the animal be-
fore the latter need make any movements to keep it in good view. The
only extra requirement is a wide cornea, and the net result is a widened
visual field.

Broad Cornece — The eflFect of an extensive cornea — and some, like
that of the house-mouse, cover about half the surface of the eyeball —
like that of large ocular size as such, is easily misunderstood. As has
been made clear, it is not true that a unit retinal area is more brightly
illuminated in a large eye {ceteris paribus) than in a small one. This
does become true only when the lens and pupil are disproportionately
large. Neither does a large cornea let in more light, as is commonly
supposed. It is the pupil which regulates the amount of light that reaches
the retina. The cornea would not need to be any larger than the fully
dilated pupil, if the iris were right against the cornea. To let light
rays hit the front part of the retina and increase the periscopy of the
eye, however, the cornea must be broader than the pupil; and the more
so, the farther the iris and lens are from the cornea. Since nocturnal
eyes tend to have deep anterior segments for the reasons given above, we
can see that their relatively broad corneas (compare lynx and man in Fig.
71, p. 173) are a consequence of these other ocular changes, and do not
in themselves promote sensitivity to light. The recession of the optical
center into the eye, in strongly nocturnal forms, cannot be wholly com-
pensated for by a broad cornea. The deeper the optical center within the
eyeball, the smaller and brighter the image will be; but the farther back
the center is from the pupil, the larger the pupil and the cornea must
become in order to maintain a wide-angled visual field. Despite all efforts
of pupil and cornea, the nocturnal eye tends dangerously toward 'tube
vision' — that restriction of visual field which we experience in looking
through an aperture located before the eye. The nocturnal animal, there-
fore, dares not rely solely upon increasing the objective intensity of the
image, by manipulating its relative size through mere gross changes in
ocular morphology and optics. He must keep the need for such changes
minimal (since they inevitably detract from visual acuity and visual
angle) by promoting the response to whatever light is available. This
necessarily means increasing the sensitivity of the retina itself.

BROAD CORNER; ROD-TO-CONE RATIOS 215

(B) The Nocturnal Retina

Rod'.Cone Ratios — We expect to find rods greatly predominating in
nocturnal retinae; and we are never disappointed. However, pure-rod
retinas are not as common among strictly nocturnal animals as pure-cone
retinae are among strictly diurnal ones. Fabulous though the cat's ability
may be for "seeing in the dark," she has a very respectable number of
cones — about a third as many as we ourselves, who are marooned among
the strongly diurnal animals when our artificial lights are taken away
from us.

This persistence of cones in nocturnal retinae calls for a Uttle special
explanation, for it has served some people as a sufficient excuse for
rejecting the Duplicity Theory entirely. The first prominent opponent
of the theory — Wilhelm Krause, a contemporary of its formulator. Max
Schultze — saw more cones than there really were in many nocturnal
forms, and drew incorrect conclusions from other animals through im-
perfect knowledge of their habits. Several modern investigators (par-
ticularly Mile. Verrier) have apparently thought that if there is any-
thing to the Duplicity Theory, then cats and owls should have no cones
whatever.

This view fails to take accoimt of the fact that whereas a diurnal
lizard never gets out of bed for a midnight snack, a cat may appreciate
a sun-bath at high noon. The nocturnal animal which wishes (as most
do) to be able to come out sometimes in daylight, is wise to retain some
cones for the improvement of form-sense, for he is otherwise at a great
disadvantage if taken by surprise by a diurnal enemy.

If this interpretation seems weak, we can surrender any positive argu-
ment in favor of a nocturnal animal's keeping cones, and still believe the
Duplicity Theory to be well founded. The only pure-rod retinae are in
nocturnal animals, and the proportion of cones in such animals is never
very high. Where there are so few as to seem utterly useless, as in the
opossum or the rat, it may be pointed out that unneeded cones are
probably harder to get rid of than are unwanted rods. The vertebrate
eye, like the brain, is so delicately-balanced an organ that it very rarely
contains anything useless. The eye is comparable to a machinery-crammed
submarine — if there is no proper niche for a thing, it is almost certain
to be in the way. In a strictly diurnal eye, even a few rods can detract
very immediately from resolving power, and they are completely elimi-
nated from every good area centralis. But cones, as we have learned, keep

216 ADAPTATIONS TO NOCTURNAL ACTIVITY

to themselves in the matter of their nerve-ceil connections, and ten cones
scattered among a thousand rods cannot cost the retina as much in
sensitivity as ten rods, scattered among a thousand cones and hooked
up to a single optic nerve fiber, would cost it in resolving power. There
is consequently simply not the urgency for getting rid of cones in noc-
turnal animals, that there is for weeding out rods in diurnal forms.
This is quite apart from any greater usefulness of 'even a few' cones
than of 'only a few' rods. The turtles are conspicuously exceptional in
having only a very few rods scattered in an almost pure-cone retina —
but even these may be useful since they are more numerous in light-
shunning forms such as Chelydra, and in the nocturnal Pseudemys.

Pure-Rod Animals — A pure-rod retina is automatically obtained
where, as in some lizards (geckoes, etc.) and snakes (Hypsiglena, Phyl-
lorhynchus) it has been manufactured by transmuting all of the single
and double cones of an ancestral pure-cone retina into single and double
rods. Transmutation has left so very few unchanged cones in Sphenodon
that in an entire section of its very large eye, never more than twenty
can be found. Aside from these forms, absolutely cone-free retinse which
once were duplex, and have lost their cones, are known for a certainty
to occur only in deep-sea fishes, the bats, and the armadillo. Some others
probably have only rods — all but one or two elasmobranchs, Lepidosiren
among the lungfishes, caecilians, the hedge-hog, the guinea-pig, the whales
and seals, most lemuroids and Aotus — but all of these need addi-
tional histological study (since most of these were last studied, micro-
technical methods have improved enormously) . Still others, like the rat
and other nocturnal rodents, are widely believed to have no cones but
do indeed have a few. One ridiculous statement often seen is that rats
and owls "have a few rudimentary cones." In a duplex retina, no visual
cell is ever rudimentary, though one population of visual cells may be so
scant as to deserve the term, like the cones of Sphenodon or the rods of
turtles. As a matter of fact, owls have enough cones so that they are
able to see more acutely by day than by night. Rochon-Duvigneaud once
picketed a Bubo bubo in an open field, and found that it could detect
an approaching hawk which was flying so high as to be invisible, at that
moment, to humans.

Summation — In nocturnal animals the rods tend to be very slender as
well as very numerous, causing the outer nuclear layer to thicken greatly
(Fig. 72, p. 177). In lungfishes and amphibians, however, the rods are

PURE-ROD ANIMALS; SUMMATION 217

bulky and exceed the cones in total volume as well as in actual numbers
(Fig. 64, p. 148) — just as in most teleosts the huge cones outweigh the
more numerous, tiny rods (Fig. 94, p. 237). The difference in acuity-
performance of bulky cones versus slender ones is obviously very great,
for the retinal limit of resolving power is set by the distance on centers
between the cones. It is not so easily apparent why nocturnal animals
should have slender rods and other animals not only fewer but plumper
ones. The slenderness of a rat's rods has not been produced for its own
sake. The distance between centers of adjacent rods has nothing to do
with the overall sensitivity of the rod population — but the number of rods
which can conveniently be hooked to a bipolar cell (this being pro-
moted by slenderness and close aggregation) has everything to do with
it. In amphibians and lungfishes not only the visual cells but most
somatic cell-types are notoriously huge. It makes an interesting specu-
lation: did the unknown factor which made their cells so large doom
the amphibians forever to low visual acuity because their cones are
usually bulky, and to a not particularly high sensitivity also, because
their rods are so big?

The thick outer nuclear layer resulting from the slenderness of noctur-
nal rods (the tiger holds the record here!) is pretty well counterbalanced
by the thinning of all other retinal layers due to the great extent of sum-
mation of visual cells in bipolars, and of these in ganglion cells, for the
sake of sensitivity and at a tremendous sacrifice in resolving ability. Noc-
turnal animals, on the whole, have thinner retinae than diurnal groups,
and have much more slender optic nerves. It is not at all unusual for
several thousand rods to be summated in one optic nerve fiber. The reti-
nal adaptations for sensitivity, both within the visual cells themselves and
in their relationship to optic nerve fibers, render the receptive tissue of a
nocturnal animal so extraordinarily sensitive to light that it cries out for
protection from any light stronger than that of the moon. We go on now
to consider how this protection has been obtained.

(C) The Slit Pupil

The elementary discussion of pupil mobility in section C of Chapter 7
was based upon the commonest form of the aperture — the circle. There
are a number of departures from this primitive shape, the most wide-
spread one being the slit, which in land animals, at least, is most com-
monly vertically oriented, for which a reason is given later (see p. 428).

218

ADAPTATIONS TO NOCTURNAL ACTIVITY

Value of the Slit Form — The slit pupil, like nearly all pupils, dilates
in dim light to a perfect or almost perfect circle. Very many years ago, a
generalization had already been found possible, to the effect that the slit
pupil is associated with nocturnal habits. Yet under nocturnal conditions
the slit pupil becomes as round as any. Obviously it has nothing to do
with vision in dim light; what then does it accomplish?

The broadly oval pupil of a frog can contract to a diameter which is
one-third of its fully dilated size; but to bring about this degree of con-
traction, the intensity of light must be increased 200 times. We have

Fig. 85 — Diagrams of mammalian iris musculatures.

a, round pupil of diurnal and strictly nocturnal forms, showing simple sphincter (solid
lines) and symmetrical dilatator (broken lines).

b, vertical slit (of cat), characteristic of nocturnal forms which bask. Part of the sphincter
surrounds the pupil, but two bundles which cross above and below and continue to the
periphery have a scissor-aciion upon the pupil, compressing it laterally. The dilatator
(broken lines) is quite symmetrical — contrast Figure 88, page 223. Redrawn from Raselli.

c, horizontal pupil (of horse), characteristic of ungulates, some whales, and other species.
Some sphincter fibers are oriented radially and are anchored in connective-tissue sectors
(stippled) which are devoid of dilatator fibers (broken lines). The pupil can expand to a
circle; but when the sphinaer fibers contract, the terminal ones force the pupil to become
a horizontal rectangle, indented by the corpora nigra (white). Based upon drawings and
descriptions of Eversbusch.

already noted that the frog is more dependent upon the photomechanical
changes of its retina for avoiding dazzlement in bright light. His pupil
cannot cope with the situation; but for that matter, neither can any pupil
whose closure depends upon a ring-shaped, sphincter muscle. We our-
selves can easily be dazzled even when our pupils are closed as far as they
will go. True, a lizard or a garter-snake is comfortable in even brighter
light despite the practical immobility of the pupil — but these forms have
only the relatively insensitive cones in their retinae.

Where the rods are very much in the ascendant, the circular pupil
ceases to be adequately protective. The sphincter may contract fully, but

THE SLIT PUPIL

219

even then it has considerable length, for it cannot eliminate itself entirely.
The arrangement of the iris muscles around a slit pupil, however, is such
as to make it easy for the slit to be closed without any impossible degrees
of muscle contraction — closed entirely in some instances, or in any case
to so small an area that the pupil is far better able to keep pace with
intensity-changes than it is in the frog or even in ourselves. (Fig. 85a, b) .
The slit pupil is hence in a sense paradoxical, for though it is an adap-
tation to nocturnaUty it has nothing whatever to do with seeing in dim
light. Hosts of nocturnal species do not have such a pupil, and are well
able to see under scotopic conditions. They get along with a circular
pupil because they are content to stay out of bright light. Any strongly
nocturnal, rod-rich animal which cares or dares to venture out in the sun,
— whether a cat stalking the barnyard sparrow, a gecko seeking flies, a

Fig. 86 — Pupil shades in mammals. After Lindsay Johnson.

a, 'umbraculum' (operculum) of hyrax, Procavia (an analogous structure occurs in many
whales), b, corpora nigra of Gazella dorcas. c, corpora nigra of camel.

snake seeking warmth, or a shark basking at the surface — needs a slit
pupil and will be found to have one.

Even some diurnal and arhythmic animals have devices for shielding
the pupil from intense glare coming directly downward or reflected up-
ward from the ground. Among such devices are the pigmentation of the
upper cornea in surface-loving needle-fishes and in Torpedo, the expan-
sible pupillary opercula of some fishes and whales (Fig. 65, p. 158), the
(voluntarily?) expansible 'umbraculum' above the pupil of the hyrax,
and 'corpora nigra' along the pupil margins of ungulates (Figs. 85c, 86).

Distribution and Meanings of Pupil Shapes — Phylogenetically, the
slit pupil is first met with in the elasmobranchs (Table VI, next page),
the only group of fishes whose pupils have much contractile excursion.
Most sharks have practically circular pupils, and a slit is characteristic

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222 ADAPTATIONS TO NOCTURNAL ACTIVITY

only of those forms which come frequently to the surface or into shallow
water — Scylliorbinus, Lamna, Selache, etc. Most of the elasmobranchs
whose eyes aim strongly upward are among the Batoidei — the skate-ray-
torpedo group. With the exception of the mantas, the batoids have oper-
cula (Fig. 65a, b; p. 158), which slope downward and slightly outward
over the pupil, and expand in bright light to block the aperture. The oper-
cular margin may be serrated, as in Raja, or smooth as in Dasyatis. It is
not unusual for rays to bask at the surface in summer, and they are then
exposed to especially strong light, considering the fact that their retinas
are pure-rod. The monk-fish (Squatina, a sort of imitation ray which is
really a shark) and the electric ray Torpedo have slits — horizontal in the
latter as in Selache and Sphyrna, diagonal in Squatina as in Scylliorhinus,
Lamna, Orectolobus, Gingylostoma, etc. At least one shark (Prionace
glauca) and some rays (e. g., Dcemomanta aljredi, Cephaloptera giorna)
have pupils which close to vertical slits. Deep-sea forms, like the less noc-
turnal of the littoral and pelagic species, naturally have roundish pupils,
which in Etmopterus and the chimaeras are extremely large and are prac-
tically immobile. The slit form of pupil is well established in the elasmo-
branchs, but in this group its orientation has never settled down to the
vertical position which is almost universal in land animals for a reason
which will appear later.

No chondrostean, holostean, or teleostean fishes have slit pupils,
though those of Acipenser and Piabuca are broad ellipses, with the long
axis vertical and with more or less of a point at each end. In the Amer-
ican shovel-nosed sturgeon (Scaphirhynchus platorynchus) the pupil is
a canted square with rounded corners. Only a very few teleosts (e. g.,
Anguilla, Encheliophis) have contractile pupils. The retinae of teleosts,
except in deep-sea species of course, are never pure-rod as are those
of practically all elasmobranchs; and moreover they have the photo-
mechanical changes to rely on. The pupillary opercula present in many
flatfishes, and ir others {e. g., Plecostomus) which live on the bottom in
shallow water, are in the same category as the umbraculum of the hyrax —
these devices are parasols for diurnal eyes which are exposed directly to
high intensities. Their mechanism of expansion has yet to be elucidated.
In one of the batfishes, Halieutichthyes aculeatus, fixed superior and in-
ferior opercula overlap as the pupil closes (taking three seconds or so to
do so), and the end result is about as in Scylliorhinus (Fig. 91, p. 225).

One lungfish, Protopterus, has a most peculiar pupil : the iris is quite
devoid of muscle elements, and yet the pupil can become a narrow hori-

PUPIL SHAPES AND THEIR MEANING

223

zontal slit. It has this form for a few hours, at least, after the animal is
released from its mud-ball or aestivational cocoon. Eventually, however,
it rounds up and thereafter remains circular in all illuminations. Another
lungfish, Lepidosiren, has a small circular pupil which never changes; but
this fish has been claimed to have photomechanical changes in the retina.
Among the amphibians, the salamanders and caecilians all have round
pupils suited to their secretive and fossorial habits. Most anurans have

a b c d efqhijk

Fig. 87 — Shape of the contracted pupil in different amphibians.

(All are circular when dilated. From various sources; right eyes; not to same scale).

a, urodeles and aquatic anurans (Pipidje et al). b, most anurans. c, Hyperlius horstockH.
d, Polypedates reinwardti. e, Corythomcintis greeningi, Aparasphenodon hrunoi, and
Trachycephalus nigromaculatus. i, several anurans (see text), g, Scaphiopus and Phryn-
omerus. h, Hyla vasta. i, Bombina. ], Pelobates fuscus. k, Calyptocephalus quoyi.

Fig. 88 — The gecko pupil.

a, eye of a gecko in diffuse daylight, x 5. After Beer, b, c, d, stages in the contraction of
the pupil of the right eye of Tarentola mauretanica. After Lasker. e, iris musculature
of T. mauretanica (combined from two figures of Lasker). Sphincter fibers suggested by
solid lines, dilatator fibers by broken lines. Note that some sphincter traas surround the
pupil concentrically and others eccentrically, while still others have a closed circuit in either
the nasal or the temporal half of the iris.

horizontal, broadly oval pupils. The rigidly nocturnal spade-foot toads
{Scaphiopus) , and the brevicipitid genus Phrynomerus also, have an
approach to the vertical slit in their beautiful lozenge-shaped pupils. The
vertical slit occurs in quite a number of nocturnal anurans — in Alytes
obstetricans, several criine toads, Lymnomedusa, Phyllomedusa and sev-
eral other bylines, some polypedatids, and Hypopachus. The Javanese
flying-frog, Polypedates reinwardti, has a slender horizontal slit, while

224

ADAPTATIONS TO NOCTURNAL ACTIVITY

Others in its family have vertical slits or broad, horizontal ovals. The
pupil is heart-shaped in Bombina, rhomboidal in some hylids, and may
take on still other peculiar forms (Fig. 87).

The crocodiles, all notorious baskers, have the vertical slit. So does
Sphenodon, in which it is tilted a bit out of plumb. The turtles are a
diurnal group with insensitive retinae and immobile, circular pupils. Most
lizards are diurnal and have round pupils; but several families of lizards
are night-prowlers and have vertical slit pupils — among them perhaps the
most remarkable of all pupils, that of the majority of the geckoes. This
pupil customarily has several tiny notches paired off along its opposite
margins. When brightly lit, the pupil closes completely, leaving a series

\

\

3^

k

tl

S'-K

s"X

Fig. 89 — Pinhole compared with a lens, as a means of forming an image.

Note that the resolution of the pinhole image depends less upon a critical location of the
screen; but the lens image is much brighter since the lens admits more light.

/- lens; p- pinhole

position of screen.

of pinholes formed by the apposed notches (Fig. 88) . Each of these pin-
holes is so small that it serves as a stenopaic aperture, forming a sharp
image all by itself just as though the lens and cornea were not there, and
moreover making accommodation quite unnecessary since it forms fairly
sharp images, simultaneously, of objects at various distances (see p. 256
and Fig. 89) . Insufficient light gets through any one of the pinholes to
stimulate the retina adequately. Since however the images formed by all
of them are superimposed on the retina, their total illumination is sufficient.
At the same time, the image is sharper than it would be if formed by a
single aperture, equal in area to the sum of the pinholes; and no sacrifice
of the width of the visual field is entailed (see Fig. 90, especially c).
Something of the same effect is obtained by Scylliorhinus (Fig. 91) and

PUPIL SHAPES AND THEIR MEANING 225

Raja (Fig. 65a, b; p. 158), and by a number of other animals (v. i.).
Among the snakes, the vertical pupil is seen in all nocturnal forms
excepting very secretive burrowers (e. g., coral snakes) and the cobras,
whose nocturnality is far from perfect. All boas and pythons, all pit-
vipers, and all vipers except such primitive and crepuscular forms as
Causus and Atractaspis, have the slit. So also with a few elapids (e. g.,

Fig. 90 — Effect of variations in the pupil. Modified after Franz.

a, standard of comparison, b, the pupil has been doubled in width, hence quadrupled in
area; but the visual field is thereby only slightly enlarged, c, the multiple pupil, whose
effect is to reduce the brightness of the image and improve its resolution, without sacrifice of
field width, d, narrowing of field owing to separation of pupil and lens, e, narrowing
of field owing to thickening of pupil margin.

Acanthopbis, Bungarus) and a considerable number of colubrids, par-
ticularly back-fanged species. In short, all strongly nocturnal snakes
which ever voluntarily hunt or bask in bright light have vertical slit
pupils. In some secretive and crepuscular forms, shapes intermediate
between the round and the slit forms occur. Thus in the rainbow snakes

"^ o ^ ^ ^ -^ ^

Fig. 91 — Eye of a shark, Scylliorhinus canicula; external view, and stages in the contraction
of its pupil. Redrawn from Franz, n- nasal side; /- temporal side.

the fully contracted pupil is a broad vertical ellipse, and in Arizona it
contracts to the shape of an egg with the narrow end pointing downward.
Diurnal snakes nearly all have round pupils, though three or four tree-
snakes (e. g., Ahcetulla picta) have horizontally oval ones; and in three
colubrid genera there is a horizontal keyhole of special significance which
may divide into two ovals when it closes (see pp. 185-6 and Fig. 79).

226 ADAPTATIONS TO NOCTURNAL ACTIVITY

Only one bird, the black skimmer {Rynchops nigra) is known to have
slit pupils, despite vague mentions, in popular and even highly technical
literature, of such pupils in owls. The pupil is most peculiar in Rynchops,
in that the two halves of the iris seem to swing inward independently,
like a pair of gates, to form the slit. One can understand the presence of
a slit pupil in a sea-bird — the surprising thing is that there are not more
such cases. Water of any depth is a dim-light environment, calling for
extra retinal sensitivity; and it is observed that the pupils of diving birds
are more responsive to light than those of others. The penguins have a
great range of pupil size. Contracted penguin pupils are never quite
round, and they can all become very small. That of the king penguin,
Aptenodytes patagonica, contracts to a perfect square, dilating through
a succession of polygonal shapes, like an iris diaphragm, to a huge circle.
It opens widely at night or when the eye is shadowed in daytime (though
the pupil of the other eye may then be a mere speck) , and it presumably
dilates widely under water. Penguins dive deeply out of sight; and
Brandt's cormorant has been trapped at forty meters, where the light is
much reduced, and is believed to go even deeper.

The skimmer does not have its sensitive eye and slit pupil for under-
water vision, however. Simple nocturnality seems to be the whole expla-
nation— the bird rests in coves by day and goes to sea in the evening to
feed all night. If this one nocturnal bird species can have a slit pupil, it
is perhaps strange that the owls, oil-birds, snipes and so on have failed to
produce one. The skimmer is scarcely the 'logical' species to be an ex-
ception in this regard, whether it be compared with nocturnal land birds
or with other oceanic birds. One would rather expect the genus of the
boobies, Sula, to have taken the lead here :

The red-footed booby, S. sula, is called by Robert C. Murphy the most
nocturnal of all sea birds. It has a notably larger eye than any other bird
in its family, but it does not have a slit pupil. A close relative, Morus
{=Sula, in part) bassana, the northern gannet, has been netted in
twenty-seven meters of water. One peculiarity of booby pupils mentioned
by one or two authors is the apparent sexual difference in size, the female
seeming to have a much larger pupil than the male. If true, this would
suggest a sexual difference in retinal sensitivity or eye-size; but Dr.
Murphy explains it as an illusion caused by a ring of black blotches at
the pupil margin of the otherwise yellow iris of the female. The male iris
being entirely yellow, the pupil seems smaller and more regular. Sula
nebouxii shows the feature strikingly; probably other boobies have it.

PUPIL SHAPES AND THEIR MEANING 227

The monotreme mammals are secretive and nocturnal, and have round
pupils. Among the marsupials, the kangaroos and wallabies are practi-
cally arhythmic, and many have oval (horizontal) pupils. New- world
marsupials, and many Australian ones, have round pupils. Other Austra-
lian species have the vertical slit. O'Day finds that some marsupial pupils,
usually described as round, do finally take on the slit form as the light
becomes sufficiently intense. Dasyurus viverrinus shows this well; but the
pupil of the more strongly nocturnal Trichosurus vulpecula becomes a
small vertical slit even in diffuse daylight of ten to twenty foot-candles,
at which intensity the Dasyurus pupil is still circular.

The placental mammals as a whole are crepuscular and nocturnal, and
shun bright light. The hoofed animals and the great cats are arhythmic,
while many primates, most squirrels, and a small handful of other scat-
tered genera (Ochotona, Zenkerella, Suricata, etc.) are diurnal. Though
the squirrels include strongly nocturnal forms (the flying squirrels) as
well as sun-worshippers, they all have round or slightly oval (horizontal)
pupils. In some of the ungulates — the camel family especially — the cor-
pora nigra of the upper and lower pupil margins (Fig. 86) can meet or
interdigitate in very bright light, perhaps forming useful stenopaic aper-
tures. In others the pupil never approaches a slit form, but can best be
described as horizontally rectangular; and it may have only slight mobil-
ity, as in the horse. The pupil of a young horse is round, but at five or
six years of age it becomes elliptical and the corpora nigra become pro-
nounced, three or four of them on the superior border and five or six
smaller ones on the inferior border of the pupil. The sheep, with as many
as twenty corpora nigra, has the maximum number of these bodies.

Large carnivores have round pupils. The foxes, all Viverridae except
Cynictis and Suricata, and one or two rodents have vertical ellipses. Out-
side of the prosimians, a fully closable slit is seen in mammals only in the
smaller cats, the strongly nocturnal and arboreal toddy cat or palm civet
(Paradoxurus) , and the dormice {Glis spp.). Paradoxurus is excep-
tional in having a horizontal slit, which has a single pair of central
notches on its margins which form a single stenopaic aperture when
the remainder of the pupil closes entirely. Two other viverrids, Cynictis
and Suricata, have horizontally oval pupils on the order of those of un-
gulates. Suricata, peculiarly vegetarian for a carnivore and rather mar-
mot-like in its behavior, is said to be diurnal.

In the cats and dormice the vertical pupil can also close entirely, leav-
ing, in the domestic cat at least, a pair of terminal pinholes reminiscent

228 ADAPTATIONS TO NOCTURNAL ACTIVITY

of those in Scylliorhinus. Seals have vertical slit pupils, excepting in one
species (Phoca barbata) whose slit is diagonal — indeed, almost horizontal
as is the slit in Paradoxums and in the hippopotamus. But the seal's
pupil, as will be made clear later, needs its slit form for a reason quite
different from the one which accounts for probably every other slit pupil
in the vertebrates.

The history of the primate group has been one of increasing diumality
from strictly nocturnal beginnings, with 'successfulness' increasing along
with the tendency toward diurnality. The range in size from the timid,
nocturnal, three-inch mouse galago to the monstrous, diurnal gorilla is
most striking. All but one of the lowest prosimians (the bush-babies,
lorises, etc.) have vertical slit pupils. The true lemurs (genus Lemur)
have vertical pupils which are not at all slit-like, but only slightly oval.
They and their closest relatives {e.g., Indr'is) do all of their sleeping at
night. All of the simians (monkeys, apes and man) except Actus are
diurnal, with the great apes most strongly so. The eyes of some pro-
simians are so sensitive that, despite the protection afforded by the slit
pupil, they are prone to undergo retinal degeneration and to become
blind when, in zoos, they are kept in too strong light. Similar changes are
said to occur, by the way, in nocturnal birds, fruit-bats, and some bears.

Tarsius is the one primitive lemuroid which does not have the slit; but
the pupil in this genus has an enormous excursion from a large circle to a
broadly horizontal oval only half-a-millimeter in diameter. In its range
of sphincter-length, the tarsier's iris has a very few close rivals : those of
the two-toed sloth, the African jumping hare (Pedetes) , the sea-snakes,
and the pearl-fish (Encheliophis) . One suspects that in such animals the
sphincter must have some special organization; but the details are as yet
unknown. They have somehow found the secret of obtaining an ex-
tremely small pupil-area without resorting to the slit form, or to the even
more elaborate device of an expansible operculum.

(D) The Tapetum Lucidum

The standard condition of the chorioid coat is one of heavy pigmen-
tation. The pigment epithelium may or may not contain much pigment
also, depending chiefly upon whether this pigment is migratory or not.
It is the pigment of the chorioid, alone, which has the real responsibility
of preventing reflections within the eyeball which might blur or even
multiply the image.

TAPETA LUCIDA AND EYESHINE 229

The light rays which are focused by the dioptric apparatus and pass
through the retina are never completely absorbed by the chorioidal pig-
ment. If they were, the ophthalmoscope would never have been possible.
With this instrument the observer looks along a beam of light which
is directed through the pupil of the eye of the subject. Enough of the
light is reflected from the subject's eyeground, directly back into the eye
of the observer, to enable the latter to see something of the retina and
the inner surface of the chorioid of the subject, magnified by the subject's
own cornea and lens.

So bright a light as that of the ophthalmoscope does not often enter
the eye directly, and the fraction of more ordinary illumination which
reflects from the chorioid is too weak to blur the principal image and
detract from visual acuity. The photographer has to rely on essentially
the same phenomenon. He has a right to expect that the dead-black
lining of his camera will reflect practically no light through or upon the
film. When such reflection does affect the film due to some defect in the
camera, the picture is blurry with the unwanted light and the photo-
grapher calls the result 'halation'.

Value and Basis of Eyeshine — There is one circumstance in which
one might conceivably strive to produce a very maximum of halation:
when the light-intensity is extremely low and a correspondingly length-
ened exposure is for some reason impossible. Cameras have occasionally
been built, in which the emulsion of the plate is on the back surface and
is in contact with a layer of bright mercury. This layer forms a mirror,
reflecting the light back through the emulsion and thus increasing its
effectiveness.

When a biologist is asked to account for the phenomenon of 'eyeshine'
in animals he may give the flip explanation : "they do it with mirrors" —
and have every assurance that he is actually being perfectly matter-of-fact
and scientifically accurate. When we consider how brightly the eyes of
many animals reflect the light of our headlights as we drive past them at
night, it is apparent that these species must be reflecting light back
through their retinae instead of absorbing it in a typically pigmented
chorioid. Ophthabnoscopic and histological investigation bears out this
suspicion, and usually discloses a special mirroring device located some-
where behind the rod-and-cone layer. Though it is very differently con-
stituted in different cases, this mirror is generically called the tape turn
lucidum. This apt term means, literally, 'bright carpet'. The tapetum is

230 ADAPTATIONS TO NOCTURNAL ACTIVITY

required by some vertebrates because of an important difference between
a camera and an eye: for the eye, exposure-time cannot take the place
of intensity — the eye can only take 'snapshots'.

Under nocturnal conditions, a visual object may be brighter than its
surroundings, or it may form a shadowy silhouette against a background
brighter than itself. There is a perennial argument as to whether a tape-
turn enhances visibility by sometimes promoting the perception of the
object, or by sometimes increasing the apparent brightness of the back-
ground. The argument is quite pointless; for, no matter which has the
greater brightness — object, or ground — the reflections from the tapetum
will increase the absolute and relative differential between the two, and
thus increase their discriminability.

Not all animals which have eyeshine possess any definite tapetum,
as an examination of the pertinent Table VII (pp. 240-1) will show. In
the ostrich, at least, the light reflex has been attributed to the lamina
vitrea between pigment epithelium and chorioid, as the lamina is extra-
ordinarily thick in this bird. A number of other birds, both nocturnal and
diurnal, also show eyeshine, but with no known structural basis for it.
There are also many fishes, anurans, and snakes (but not lizards) in
which there is eyeshine and in which the reflecting material has not
been identified, though it is certainly nothing especially differentiated
for the purpose.

An anomalous eyeshine even occurs in a few humans. It is normally
lacking in all diurnal monkeys and apes, and Ernest Walker found only
a "faint suggestion of a shine" in the diurnal Lemur catta. Among the
other mammals, the rodents and lagomorphs are conspicuous for having
a dull eyeshine (whose basis is yet to be found) in nearly all species,
including even the strongly diurnal squirrels. Only one rodent, Cunt-
cuius paca, is known to have a tapetum; and even here the reflex is said
to be of only moderate brilliance. The Hystricidae may prove to have a
tapetum of some sort, for in these exotic porcupines the silvery eyeshine
is described as being particularly brilliant, and visible through a wide
angle.

In snakes, the eyeshine varies from faint to brilliant in both diurnal
and nocturnal groups. Klauber states that it can be seen through only a
narrow angle, which suggests that it may come wholly from the myelin-
ated optic-nerve head and means nothing to the scotopic vision of the
animal.

EYESHINE; THE TAPETUM FIBROSUM 231

Wherever special tapeta have been constructed for reflecting light
back through the visual cells, they are most often located in the chorioid
coat just behind the retina; but they may be retinal, placed in the pig-
ment epithelium of the retina itself.

The light reflected from a chorioidal tapetum, of either the 'fibrosum'
or 'cellulosum' type (v, /".), is ordinarily seen only if the observer is
stationed beyond the animal's near point. With large animals which
have little or no accommodation, this means not closer than from eight
to twenty feet. The light is always colored though unsaturated, some-
times so greatly as to appear almost white; and the hue may be situated
practically anywhere in the spectrum except in the violet. The color may
vary within a species or even, from moment to moment or from day to
day, in the same individual. Such variations are unquestionably due to
fluctuations in the amount of blood in the choriocapillaris, in the amount
of rhodopsin present, etc., through which the light reflected by the tape-
tum must pass to escape again from the eye. The fundamental color
thrown back from a chorioidal tapetum owes its hue to the interference
of light, for it is a surface color like that of a beetle's wing-cover, a
parrot's feather, or a film of oil floating on water. The hue depends upon
the microscopic dimensions of the reflective elements and has no biolog-
ical significance as far as one can tell.

Retinal tapeta usually appear pure white ophthalmoscopically, though
the eyeshine of crocodiUans is said to be pinkish-orange (and extremely
brilliant in Caiman sclerops) . Didelphis virginiana is also described as
having a tinted (orange) reflex. With retinal tapeta, the glow can still
be seen when one is very close to the animal — less than a foot, in croco-
diUans, if one cares to go that close. The whiteness of retinal tapeta
makes it possible to see, ophthalmoscopically, the red shimmer of rho-
dopsin against the background of the tapetum in a dark-adapted speci-
men. Rhodopsin was first seen in this way, in the living eye, in crocodiles
and in a freshwater fish, the European bream (Abramis bratna) .

The Tapetum Fibrosum — The simplest kind of tapetum lucidum is
the fibrosum type. Nearly all hoofed animals have this kind, most
tapeta fibrosa are in such animals, and none of them has any other kind.
A portion of the thickness of the chorioid, just outside of the chorio-
capillaris layer, has simply been converted from an areolar type of
connective tissue to a tendinous sort, and glistens just as does a piece
of fresh tendon. The tapetum fibrosum is composed of dense, regular.

232

ADAPTATIONS TO NOCTURNAL ACTIVITY

fibrous tissue, with the pigment cells and large blood vessels proper to
the chorioid cut down locally to a minimum or eliminated. Of necessity,
chorioidal tapeta are perforated at intervals by capillaries running ver-
tically through their thickness to supply the choriocapillaris (Fig. 92b,
c). The arborizations of these into the choriocapillaris are visible with
the ophthalmoscope as stellate black dots on the bright background of
the tapetum — the so-called stellulae Winslowi.

The tapetalized area of the chorioid, in most ungulates and carnivores
(which together include a great majority of all tapetum-bearing animals)
is roughly a triangle with its base horizontal, and either including or
avoiding the disc. The rounded apex, in the superior part of the fundus

.>S:5---

s#=-

Fig. 92 — Mammalian tapeta lucida, histological. From Franz, after Murr (ms

a, bundle of fibers from tapetum fibrosum of the ox, Bos taurus. b, chorioid of
vulpes, showing modification of inner layers to form a tapetum cellulosum.

p- pigmented portion of chorioid; /- tapetum cellulosum; c- capillary supplying

capillaris; cc- choriocapillaris.

)•
Vulpes

chorio-

of the retina, makes about a right angle and the other two corners are
not much less broad — being a spherical triangle, the tapetum can of
course have angles totalling much more than 180°. The fibers of the
tapetum are arranged in close-set concentric rings so that the entire
tapetum is a single many-layered whorl of spindle-shaped fibers. Over
the region occupied by the tapetum, the retinal pigment epithelial cells
are devoid of pigment granules, thus interfering minimally with the
passage of light back and forth through them.

A tapetum assignable to the fibrosum category, though of course
independently evolved, is known in a few fishes and will no doubt
eventually be found in many others. Our American fishes are most im-

THE TAPETUM CELLULOSUM

233

perfectly known, ophthalmologically speaking. Such forms as the moon-
eye (Hiodon) probably have tapeta of some sort, possibly tapeta fibrosa;
but they have not yet been studied.

At least two or three of the marsupials have produced tapeta fibrosa.
Those of the elephants and whales, however, may be genetically related
to the tapetum of the ungulates, of which both groups are sometimes
considered to be remote kin. In the broadest sense of the term, the
elephants are ungulates. The whale tapetum differs from that of a
hoofed creature only in being thicker and more extensive in area, though
it is usually restricted to the superior half of the retina.

The excellent tapetum fibrosum of Aotus (= Nyctipithecus) , whose

Fig. 93 — ^Tapeta lucida in surface view.

a, fundus of carnivore (dog; right eye), showing characteristic shape of tapetum cellulosum
(hatched) and usual location of disc (stippled); the tapetum fibrosum in ungulates has
about the same extent, but is more rounded dorsally and tends toward a semicircle in shape.
Redrawn from Preusse. b, single cell from tapetum cellulosum of domestic cat, showing
rodlets of reflective material. Redrawn from Murr. c, shape and extent of tapetum of the
common opossum; the drawing could serve fairly well to represent the whales and the one
tapetalized rodent, Cuniculus paca; but the tapeta of seals are even more extensive.

eyeshine is reported to be more brilliant than that of the cat, represents
another independent concoction of the fibrosum type. These douroucoulis
or night-monkeys are the only nocturnal Simiae — thus, the only nocturnal
New World primates — and the tapeta of the Prosimiae belong to quite
another category:

The Tapetum Cellulosum — Besides the tapetum fibrosum, another
equally widespread chorioidal type is the tapetum cellulosum. The noc-
turnal prosimians (whose eyeshine is especially vivid) , all but two species
of the great order Carnivora, and all of their close relatives the seals,
have been found to possess this more complex type. The glorious eye-

234 ADAPTATIONS TO NOCTURNAL ACTIVITY

shine of the domestic cat has been known literally for millennia : it was
the basis of the reverence shown the cat by the ancient Egyptians, who
believed that the cat's eyes magically reflected the sun even at night
when it was hidden from mere man. Although the typical carnivore
tapetum is the same large triangle as the tapetum fibrosum of an un-
gulate (Fig. 93a), and resembles it ophthalmoscopically even to the
presence of the 'little stars of Winslow', it is very different histologically
and in evolutionary origin :

Endothelial cells, such as lurk in the meshes of any chorioid, have
proliferated just outside of the choriocapillaris to form several layers
of thin, broad, tile-like cells (Fig. 92b) . Unlike the arrangement of cells
in a true stratified epithelium, there is a tendency in the tapetum cellu-
losum for the boundaries of each cell to coincide with those of cells in
the layers immediately above and below — in other words the courses of
brickwork are not staggered. The connecting capillaries, running to the
choriocapillaris from vessels in the outlying, normally vascular, pig-
mented layers of the chorioid, can consequently take quite straight
paths and thus interfere but little with the action of the tapetum.

The number of layers of cells may be only four or five, as in the
wolverine, or as many as 15 as in the cat (the dog has 10, the lion 8
to 10). The numbers are higher in the seals, however, ranging from
16-18 to 30-35 (in Phoca barbata). In one seal (Halichoerus gryphus)
the tapetal cells are so elongated as to simulate a tapetum fibrosum; but
they are still cells, not inert connective-tissue fibers as in a true tapetum
fibrosum. The seal tapetum covers a great area of the retina, usually
extending at least to the equator of the eyeball in all meridians and often
much farther than this on the temporal side, the retinal region which
looks ahead of the animal. This record-breaking area of tapetum in the
seals will appear significant when we consider its special purpose in
these animals (pp. 446-8).

Though the elements of a tapetum cellulosum (unlike those of the
true fibrosum type) are Uving cells, there is not room in them for much
protoplasm. They are packed with highly refractive threads or rodlets,
in some cases long and with crossings and recrossings to form a felt-
work, in other cases very short and set in serried rows so that a 'herring-
bone' pattern is created (Fig. 93b). These inclusions are formed of
some organic substance, perhaps different in different cases, whose
chemical nature is unknown; but they appear to be crystalline and homo-
geneous. In the cat they are yellowish, about 10[X by 0.5-1 [1, and

GUANIN AND THE ARGENTEA 235

apparently compounded of still smaller elements. Those of the seals
have been found to resist weak (but not strong) acetic acid, and are
blackened by osmic acid, suggesting a lipoid nature which their double
refraction confirms.

Guanin and the Argentea — The best known of the retinal tapeta
lucida — called pseudo-tapeta by Briicke, who published the first exten-
sive description of tapeta lucida in 1845 — are those in which the pigment
epithelial cells contain masses of particles, or crystals, of guanin. This
substance is also employed in chorioidal tapeta, which otherwise resemble
the mammalian tapetum fibrosum. Guanin plays the essential role in the
amazing tapetum of the elasmobranchs, and it is employed in an alto-
gether different kind of mirror located on the outside of the eyes (and
bodies) of fishes. It deserves more than a few words on its own account :

Guanin is chemically a purine, and is closely related to uric acid. In
extracted form it is an uninteresting, pale yellow, chalky powder; but
when deposited, either as simple guanin or as the calcium salt, in the
right places and in the right way, it can endow living tissues with the
metallic lustre of silver or gold. Guanin has long been employed, wher-
ever a mirror was needed, by fishes and a few higher vertebrates. Before
them, invertebrates had used salts of uric acid to form concentrating
mirrors in light-producing organs, which are often built much like an eye.
The silvery sides of a minnow are plated with guanin-laden scales.
Indeed, the name of the substance comes from 'guano', the term for the
excrement (of Peruvian cormorants) which is mined for fertilizer on the
sea islands where the piscivorous guanay-birds of millennia once piled
it a hundred feet deep. Before it has been through the alimentary canal
of a bird, the guanin of fish scales is known commercially as argentine,
and under the name of 'essence d'orient' it was formerly used in the man-
ufacture of artificial pearls.

The entire uveal tract of a fish eye becomes jacketed, in the larva,
with a guanin-laden outer layer called the argentea. Just as the silver
reflections from an adult fish's sides blend with the bright water surface
when seen from below by a predator, so does the argentea of a larval
fish eye render that eye inconspicuous within the glassy body, by con-
cealing the black pigment of the uvea which has already developed so
that the little eye can function. This interpretation of the argentea as
an embryonic adaptation to light is confirmed by the fact that it is
seldom found in fishes which live in the darkness below 400 meters.

236 ADAPTATIONS TO NOCTURNAL ACTIVITY

As the fish grows up and the head tissues become opaque, the argentea
covering the chorioid loses most of its meaning, though in the enucleated
eye it can still be seen shining through the transparent sclera. Where
it continues over the face of the iris, however, it has been claimed to
serve as a mirror, reflecting light (enough?) toward crannies and crevices
into which the fish happens to be trying to look. The head-mirror worn
by a physician, which he pulls down so that the hole in it is opposite his
eye when he wants to peer down our gullets, might have been copied by
its inventor, Czermak, from the argentea layer of a fish's iris. Whether
useful in this way or not, the iridic argentea naturally adds to the opacity
of the iris (Fig. 67, a, p. 159). By reflecting much of the light, the
guanin leaves less for the melanin of the rather thin fish iris to absorb.

Guanin in Retinal Tapeta — One of the cleverest uses of guanin is
in the retinal tapetum lucidum seen in a few European freshwater fishes
and very recently found by George Moore in one of our native species,
the pikeperch Stizostedion vitreum. Known in Abramis brama for about
a century, and in Rutilus rutilus and Lucioperca sandra for decades,
this type of tapetum has been described by its chief student, Wunder,
also for Blicca bjorkna, Pelecus cultratus, Acerina cernua, Lucioperca
yolgensis, and (provisionally) for Abramis ballerus and Acerina
schratzer. Wunder found all of these fishes in Lake Balaton, in western
Hungary. Some of them are the most abundant of the 37 species of
fishes in that unusual body of water. The 'Balatonsee' is peculiar in that,
while enormous in area, it is everywhere shallow — averaging 6 feet in
depth; and its waters are turbid almost to the point of opacity for nearly
the whole of the year. These tapetum-bearing fishes are quite definitely
adapted to this environment, but were of course pre-adapted (see p. 388)
before ever they got into it, for most or all of them occur elsewhere in
Europe as well. Moreover, the above assemblage of fishes represents at
least two separate productions of the same sort of tapetum, for some of
the genera {Abramis, Rutilus, Blicca, Pelecus) are cyprinid, malacopter-
ygian, fishes; while /4cenn£7 and Lwciopercc? (the latter a close relative of
our Stizostedion) belong to the perch family among the Acanthopterygii.

The retinal guanin tapetum may be small, or may form a huge hori-
zontal oval area which practically fills the fundus. It will suffice to
describe it for one of the best-known cases, and figure it for another :

In the superior two-thirds of the fundus of Abramis brama, a normal
amount of fuscin pigment is present in each retinal pigment epithelial

GUANIN IN RETINAL TAPETA 237

cell. Along with it, partway down the length of the cell-processes, is a
cloud of guanin crystals (Fig. 94) . The pigment migrates in the usual
way, retracting into the body of the cell in the dark and moving far
down into the processes in the light (pp. 146, 149). As the fuscin granules
surge on their way in either direction, they infiltrate among the guanin
crystals, leaving the latter relatively undisturbed in position — indeed, the
guanin may migrate to some extent in the opposite direction. Contract-
ing behind the guanin layer in dim light, the pigment exposes the crystals

Fig. 94 — The occlusible retinal guanin tapetum of certain teleost fishes, as exemplified by
the European pikeperch, Lucioperca sandra. x 500. Redrawn, modified, after Wunder.

a, visual-cell layer of light-adapted retina, showing cones contrarted to limitans, rods elon-
gated, and retinal pigment (black granules) expanded into the heavy pigment-cell processes
to mingle with the guanin (silver), destroying its effectiveness as a mirror (c/. Figs. 62, 63,
64, pp. 146-8).

b, dark-adapted situation, showing rods contracted toward limitans, cones elongated, and
retinal pigment retracted into pigment-cell bodies to expose a guanin mirror distal to the
mass of tiny rods.

pecb- pigment epithelial cell bodies; r- rods; c- cones; onl- outer nuclear layer.

to serve as a reflective backing for the mass of rod visual cells. Migrating
past the guanin in bright light, into a position between it and the light,
the fuscin covers up the guanin layer. No light is then returned through
the visual cells, after having once traversed them.

This type of tapetum may be said to be occlusible — that is, capable
of being occluded or covered up in bright light when it is not wanted.
It is thus fundamentally different (physiologically) from the tapeta of
Evermannella and other dim-light fishes in which the pigment epithel-
ium is crammed with guanin but contains no migratory dark pigment

238 ADAPTATIONS TO NOCTURNAL ACTIVITY

with which to cover it up — all of the fuscin being concentrated in small
masses in the tips of the pigment-cell processes, as in the sturgeons (v.i.).

A retinal (guanin?) tapetum is common in bathypelagic teleosts; and
it may be occlusible in the young, which characteristically live much less
deeply than the adults, and have both reflective material and fuscin in
their pigment cells. The fuscin disappears during growth, so that the
adult tapetum is certainly fixed. Like the argentea, the tapetum is lacking
in bathybic teleosts which never come near the surface.

The guanin tapetum formed in the pigment epithelium of the croco-
diles and their allies is non-occlusible, for the cells contain much guanin
and only a little fuscin, which migrates but feebly and is inadequate to
blanket the guanin from the light. If we assume that the guanin was put
there early in the evolution of the group, before the photomechanical
changes dwindled as they have in these reptiles (p. 162), we can imagine
that the crocodiles once had an occlusible tapetum but found it unneces-
sary to maintain it once they had developed an efficient vertical-slit pupil.

Other Retinal Tapeta — Other non-occlusible retinal tapeta are those
of the fruit-bats and that seen in the common opossum, Didelphis vir-
giniana (but not in Marmosa, though all opossums have eyeshine). The
opossum structure occupies the superior half of the eye-ground, and is a
neat semi-circle with its straight margin running horizontally at the
level of the disc (Fig. 93c) . The pigment epithelial cells below this level
have their normal, dense content of fuscin granules; but in the modified
area (Fig. 95) they are twice as tall, devoid of pigment, and packed full
of microscopic particles which look like guanin but apparently are not.
These granules dissolve readily in histological reagents which guanin
resists, and are hence not seen in micrological sections of opossum eyes.
The pale yellow particles with which the pigment cells of the fruit-bats
are filled are likewise of unknown chemical composition. In the dog, the
retinal pigment epithelial cells covering the tapetized part of the chorioid
are themselves filled with reagent-resistant reflective particles, which have
never yet been accurately studied or described.

Guanin in Chorioidal Tapeta — Guanin also occurs in chorioidal
tapeta. That of the sturgeon bears a superficial resemblance to a tapetum
cellulosum, with up to twelve layers of cells; but the cells are filled with
guanin or a closely related substance (Fig. 96) . The pigment epithelium
has not been able to rid itself entirely of pigment in the portion which
overlies the tapetum. Instead of there being a little pigment in each cell

OTHER RETINAL TAPETA

239

however (as in a couple of poorly developed ungulate tapeta) there may
be none at all in most of the cells. An occasional cell contains consider-
able pigment in the cell-body (European sturgeons) or a great deal of
pigment compactly massed in the tip of a very heavy process (Acipenser

»

■*i,it

Fig. 95 — Retina of the common opossum, Didelphis virginiana. x415. After Walls.

a, from the upper part of the tapetalized region (compare Fig. 93c), showing modification
of the pigment epithelium; a very few pigment granules are present, along with a mass of
reflective material, in this part of the tapetum (note capillary against external limiting mem-
brane, at right), b, from the inferior fundus, showing unmodified, heavily pigmented pig-
ment epithelium, contrasted with the tapetum in a (t) by the alignment of the external lim-
iting membrane in the two photos.

fulvescens — Fig. 96). The effect is as though all the cells had pooled
their pigment in a scattered minority of their number, in order to min-
imize the obscuration of the tapetum. The elements of the tapetum
fibrosum in some marine teleosts (most of them bathypelagic) contain
large masses of guanin, which were formerly called 'ophthalmoliths'.

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242

ADAPTATIONS TO NOCTURNAL ACTIVITY

Fig. 96 — Retina and tapetum of the rock sturgeon, Acipenser fulvescens. x 500.

(The large retinal pigment cells each contain pigment. More commonly, in other sturgeons,
the cells are small and only a few contain any pigment).

b,a- bipolar and amacrine cells; c- cone (c/. Fig. 22a, p. 54); cc- choriocapillaris; g-
ganglion cells; gm- glass membrane; gt- guanin tapetum, occupying inner portion of
chorioid; he- horizontal cells (massive, non-conductive type); pc- pigmented portion of
chorioid (largely out of the piaure); pp- pigment-filled process of pigment epithelial
cell: T- rod.

GUANIN IN CHORIOIDAL TAPETA 243

The guanin tapetum in the elasmobranch chorioid is occlusible, and
is much the most remarkable of all tapeta lucida despite the fact that its
owner is the most primitive living vertebrate type to have a tapetum of
any kind. While in other vertebrates the chorioidal pigment cells have
at best little ability to change their shape, the elasmobranchs have spe-
cialized a layer of such cells whose pigment has extraordinary migratory
capacity, in every way equal to that of a teleost retinal pigment cell or a
dermal chromatophore. The bodies of these cells form a mosaic toward
the inner surface of the chorioid, each with a plate-like process running
slantwise (over most of the area of the chorioid) to the choriocapillaris.
The processes thus overlap like shingles set at 45° (Fig. 97), and along-
side of them are flat guanin-filled cells. In dim light, the migratory pig-
ment retracts into the body of the cell. Light rays which pass through
the visual cells and the smooth, pigment-free pigment epithelial cells,
now strike the guanin and are thrown back through the visual cells again.
In the light, the migratory chorioidal pigment expands so that light rays
now strike pigment, instead of the guanin, and are absorbed without
reaching the latter. The arrangement works, it is to be noted, only be-
cause of the slanted position of the alternating plates of guanin and
retractible pigment. There is a strip of chorioid, usually horizontal and
always superior to the optic disc, in which the guanin plates are not
slanted. Here, locally, the tapetum is fixed and non-occlusible. The one
known area centralis in selachians — that of Mustelus (Fig. 77a, p. 185)
— is located within the non-occlusible region. An area centralis (for
acuity) and a tapetum (for sensitivity) are of course not incompatible,
as is obvious from the situation in the ungulates and carnivores (v. i.,
and note, p. 185). In at least three elasmobranchs the tapetum is under-
standably lacking : Lcemargus is an abyssal shark, Myliobatis is a pelagic
ray which has cones as well as rods; and the basking shark (Selache
maxima) basks a good deal, as its name implies.

Phytogeny and Relative Efficiency of Tapeta — One naturally
wonders which of these various types of tapeta is most effective; and,
if any one is outstanding, why any other types were ever produced. The
potentialities of all tapetal types are apparently present in the fishes; but
the above questions are quite impossible to answer at present. It seems
surprising that so ingenious a device as the elasmobranch tapetum should
not have persisted all the way to the mammals — or at least have been
re-invented one or more times. But it must be remembered that diurnality

244

ADAPTATIONS TO NOCTURNAL ACTIVITY

and nocturnality come and go in evolution as mutatory capacity and
ecological expedient direct. Each return to diurnality in a given line of
descent will abolish any pre-existing tapetum. Upon a subsequent swing
toward nocturnality, the group starts from scratch and is as likely to
hit upon one device as another, where so many solutions to the same
problem are possible. In no other way can we account for the spotty

visual cells here

visual cells here

Fig. 97 — The occlusible chorioidal guanin tapetum of the elasmobranch fishes.
Semi-<diagrams based upon Mustelus mustelus as figured by Franz.

The guanin is shown in silver. At the left: sagittal seaion through the chorioid of a light-
adapted eye, showing pigmented processes expanded over the proximal surfaces of the guanin
plates, shielding them from the light which has passed through the retina. At the right:
dark-adapted condition, showing pigmented processes retracted to allow the guanin to reflea
light back through the visual cells.

cc- choriocapillaris; gp, gp- guanin plates; n- nucleus of guanin cell; pc- layer of migratory
chorioidal pigment cells; pe- pigment epithelium of retina (devoid of pigment); pp,pp-
pigmented processes which can be advanced and withdrawn; uc- unmodified portion of
chorioid (largely out of the picture above; shows ordinary flat, static pigment cells).

distribution of tapeta as such, and of each type thereof. Only in the
Carnivora-Pinnipedia is it likely that a pair of large taxonomic groups
share a tapetal type in common by virtue of inheritance from a common
ancestor.

At present, no one can arrange tapeta in any order with respect to
their reflection coefficients, their efficiency as mirrors. Apart from the
manifest superiority of occlusibility, there is only one factor in whose

PHYLOGENY, EFFICIENCY; TAPETA AND ACUITY 245

variations we can see an obvious effect upon tapetal efficacy. This is the
distance of the reflective material from the tips of the visual cells. Where
this distance is greater, as in chorioidal tapeta (separated from the tips
of the rods by the thickness of the choriocapillaris and the pigment epi-
thelium), the spreading of the scattered reflected light results in its
striking many rods in addition to those which it had originally traversed
before reflection. Where the tapetum smoothly and directly contacts the
visual-cell palisade, as in the opossum, there is less opportunity for scat-
tering to blur the image and detract from the acuity of scotopic vision —
low, at best, as it is bound to be. Yet the opossum gives every evidence
of having extremely low visual acuity, while the cat is far from being
badly off in this respect (see Table V, p. 207). If there were anything
logical about the distribution of tapetal types, the cat would have the
opossum's, and the opossum, the cat's.

The Tapetum and Visual Acuity — The tapetum is not always re-
stricted in usefulness to the dimmest of illuminations. As was pointed
out in Chapter 7, the all-round capacity of twenty-four-hour eyes is not
due to a fence-straddling avoidance of specialization, but to a mosaic
of compatible specializations for both scotopic and photopic vision.
A tapetum is perfectly compatible with an area centralis (though it is
never associated with a fovea). Mustelus is matched, among the prim-
ates, by Lemur catta and Aotus. One of these is diurnal, the other noc-
turnal; but each has both an afoveate area centraUs and a tapetum, while
the close relatives of both (other Lemur spp., other Simiae) have neither
of these features.

Notably, the ungulates and some carnivores (lion, polar bear) have
large eyes but not particularly small images. They can compensate for
the dimness of the large image by means of the tapetum, the size of the
image enabling them to attain keen vision despite the low ratio of cones
to rods. In dim light the tapetum gives the animal enough sensitivity,
and in average light it is still usable because of the size of the image. It
is certainly not ordinarily a source of dazzlement as is evidenced by the
fact that few ungulates and no large carnivores have any approach to a
slit pupil. It is probably no accident that in these animals the area cen-
tralis falls within the confines of the tapetum. If cones are indeed concen-
trated within these imperfectly known areae centrales, the lowered sensi-
tivity of those regions is nicely compensated by the tapeta behind them.

246 ADAPTATIONS TO NOCTURNAL ACTIVITY

We do know that the visual acuity of ungulates is far higher than we
would expect to find in the average tapetum-bearing nocturnal animal
with its rod-rich retina — the average dog-sized carnivore, for example —
despite the rather large absolute size of the eyes of foxes, cats, and the
like. The old-time Arab horse breeders are said to have invented a game
in which the winner was he whose horse recognized him, from upwind,
from the greatest distance — showing its recognition by heading straight
for its master who stood with the other owners in a great semi-circle at
a considerable distance. The champion seems to have been a horse which
recognized his master from 500 meters away. And the vision of the horse
is superb by night as well as by day. An Arabian fable cited by Rochon-
Duvigneaud runs like this : "The Lion and the Horse were arguing as
to which had the better vision. The Lion, on a dark night, could see a
white pearl in milk — but the Horse could see a black pearl amidst coal.
The judges decided in favor of the Horse."

Another empirical example, which could hardly be improved upon,
is that given in the observations made by an old hunter on the prong-
horn (Antilocapra americana), and quoted by Seton: "What a live
antelope don't see between dawn and dark, isn't visible from his stand-
point; and while you're a-gawkin' at him through that 'ere glass to make
out whether he's a rock or a goat, he's a-countin' your cartridges and
fixin's, and makin' up his mind which way he'll scoot when you dis-
appear in the draw for to sneak on 'im — and don't you ferget it."

Chapter 10

ADAPTATIONS TO SPACE AND MOTION

(A) Accommodation and its Substitutes

Any object in visual space may have a number of perceptible attri-
butes: size, shape, pattern, brightness, color, position, motion, and dis-
tance. Our awareness of most of these derives fairly directly from the
character of the retinal image itself, whose size and shape, tempered by
experience and memory, tell us the 'true' size and shape of the object.
We translate subjective luminosity into objective intensity, making un-
conscious allowances for our adaptation-condition and for the illumin-
ation of the moment. A white object thus seems white even when it is
reflecting less light than some black object seen under other conditions.
So also with color, which remains remarkably constant in our minds even
though the illumination be qualitatively altered. Pattern resolves into
variations of brightness and color, motion into a varying stimulation of
successive retinal regions.

Dependence of Apparent Distance upon Size — When we consider
distance however, we are dealing with an object-attribute concerning
which the retinal image, alone, can give us no information whatever. A
light ray is a straight line, and when one end of that line lies in a visual
cell the physiological result is the same no matter how near or how far
the other end of the line may be. For our knowledge of the distance of
a visual object, we are much more dependent upon past experience than
upon what our eyes can tell us at the time.

To know either the size or the distance of an object, we must know the
other. If we do not know one of these facts, we do not know either. The
farther an object is, the smaller its retinal image and the smaller its
apparent size. If it looks small and we know it to be large, we judge it
to be far away. If it looks large and we know it to be small, we judge it to
be close at hand. Brightness, haziness, overlapping of other objects, per-
spective, vertical position with respect to the horizon, and parallax are
other factors in monocular judgement of distance; but like size itself,
most of these are in a sense interchangeable with distance and can aid us
to accurate estimations of distance only in so far as they themselves are

247

248 ADAPTATIONS TO SPACE AND MOTION

accurately evaluated. Thus, strangers in mountainous country underesti-
mate distance because of the exceptional clearness of the air — in their
experience, objects look that sharp only when they are nearer. Similarly,
distances through mist and fog are easily overestimated, since ordinarily
such ha^y outlines and unsaturated colors connote greater distances.

An amusing and convincing demonstration of this interdependence of
size- and distance-judgements is the following experiment, which the
reader can make without travelling to the Rockies or waiting for a fog :
Stand before a large mirror with arm outstretched before you, index fin-
ger pointing upward. Watching the finger closely, move it toward you
and away from you, noticing your reflection in the mirror all the while
but without taking your attention off of your finger. As the finger ap-
proaches your face, your image in the mirror will appear to shrink and
recede; and when the finger is moved toward the mirror your reflection
will seem to advance and expand.*

The point is that judgement of distance is very largely subjective and
is very easily deceived. This, despite the fact that the eye may make a
thoroughly objective and very precise adjustment to the distance of the
object to which we are giving attention, the adjustment called accom-
modation. If nature has anywhere fallen down very badly in designing
our visual mechanism, it is in neglecting to tie our awareness of distance
firmly to our neuromuscular apparatus for adjusting to it, which would
have put the estimation of distance upon an objective basis. However,
nature may be pardoned on this score so far as we humans are concerned,
for we have binocular vision at a maximum and gain a potent cue to dis-
tance, from the convergence which our eyes automatically perform along
with their accommodation, and which takes place even beyond the limit
of distance within which accommodation is necessary for most of us.

It is not distance as such, or its variation as such, that makes accom-
modation necessary. Some animals get along nicely without it, even
though they may be standing alongside of others which are utterly de-
pendent upon accommodation for maintaining an equally sharp image
of an object at which both are looking. The need for accommodation, or

*Explanation: As the finger nears your face its retinal image enlarges; but since your atten-
tion is steadily upon the finger, which is very familiar to you and whose size you know to be
constant, you see it as having the same size as ever. By contrast, however, the motionless
image of your whole body, over which the finger is superimposed, becomes relatively smaller
and is hence perceived as shrinking in size. And, since in your experience decreasing (or
apparently decreasing) size always means increasing distance, your image seems to recede
farther behind the mirror. As the finger is moved away these processes are reversed and the
mirror image apparently enlarges and comes toward you.

DISTANCE AND SIZE 249

the lack of need, resides in the plan of the eye itself and not in the dis-
tance of the object.

The Why of Accommodation — The ideal human eye, in a state of
internal rest, is said to be emmetropic. By this is meant that parallel rays
of light, striking the cornea through air, are brought to a point focus on
the retina (Fig. 12, p. 27). It needs to be emphasized that the average
human eye is not emmetropic. Emmetropia is decidedly the exception,
not the rule. The most prominent student of mammalian refraction,
Lindsay Johnson, found a slight and beneficial degree of hypermetropia
in the eyes of primitive peoples, and considered that this might be the
truly normal human situation.

In emmetropia, if we should gaze at the sun for a long moment, a tiny
hole would be burned through the retina in the region of the fovea — the
focus of those intolerably intense, parallel rays. If we set up an experi-
mental source of milder parallel rays in a dark-room, it can be at any
distance beyond twenty feet and will theoretically always have the same
brightness, for the same sized light-pencil (just filling the pupil) will be
brought to a point focus.

But natural objects are not giving off parallelized beams of light. From
each point on the object, rays diverge away in many directions and only
a few of them are aimed at the pupil of a nearby eye. Unless these are
brought to a point focus in the layer of visual-cell outer segments, we
will not see that object-point as a point and cannot build up a sharp
retinal image of the object (Fig. 10, p. 25). The light by means of which
we see the object-point is thus a cone, its apex the object-point and its
base the pupil — or more accurately, that circle of cornea from the circum-
ference of which rays bent by the corneal surface can just enter the pupil.

As the object approaches, the cone of light entering the eye from each
point on it becomes a shorter, stubbier cone with a much greater angle at
the apex, so that more of the light rays emanating from each point are
now caught by the pupil and the object looks brighter. But these rays are
now striking the corneal surface at lesser angles than before and if the
ray-bending (focusing) power of the eye remains unchanged, the point
at which they are brought together will move backward in the eye and
slip off the tips of the visual cells into insensitive pigment epithelium.
The eyeball being then too short, its vision becomes like that of a hyper-
metropic or far-sighted eye (Fig. 12), and the visual cells register only
blur-circles. To bring the crisp image forward into the visual-cell layer

250 ADAPTATIONS TO SPACE AND MOTION

again, either the optical center of the eye must be moved forward, farther
from the retina, or else the ray-bending power of the dioptric apparatus
must be increased — by sharpening the curvature of the lens, the cornea,
or both.

Both of these general methods of accommodation — by moving the lens
(Figs. 98 and 99) or by increasing its curvature (Fig. 100) — are in use
among various vertebrates. Through evolution, there has been a tendency
to abandon the first method for the second, simply because of greater
ease of making it mechanically precise and positive, rather than because
of any inherent optical superiority of the one method over the other.

Accommodation is necessary, then, to keep a sharp image of an ap-
proaching or receding object within the thickness of the visual-cell layer.
The word as used by medical men refers only to the adjustment for ap-
proach or static nearness, but this application is hardly broad enough for
our purposes; for, in some vertebrates, the resting eye is myopic, making
a saving of muscular effort since the eye is used mostly at close range.
Parallel rays are then focused in front of the retina, and the lens must
be moved backward to adjust for a distant object — a 'negative' accom-
modation as compared with our own (Fig. 98).

Obviously, the need for accommodation depends upon two things : the
amount of forward or backward shift of the image relative to a given
shift of the object, and the length of the visual cells. When an emme-
tropic human eye fixates an object at the horizon, its image falls some-
where in the layer of outer segments — presumably very close to their
inner ends. Now, that object can approach the emmetropic eye to a dis-
tance of only twenty feet without its image moving backward a distance
greater than the length of the outer segments — a tiny fraction of a mill-
imeter. The approach of the object is thus minified far more than are any
sidewise movements it may make. The image moves backward faster and
faster, however, as the object comes up; and when it comes within twenty
feet the lens must begin to sharpen its curvature to keep the optical image
coinciding with the photochemical image in the outer segment layer.
When we have sharpened the curvature of the lens as much as we can,
and the object is still clearly seen, it is said to be at our 'near point' —
which may be a few inches before our eyes if we are young, or beyond
comfortable arm's reach if we are middle-aged and 'presbyopic' When
we are very old and the lens is too hard to deform at all, the near point
has of course receded from us to the twenty-foot distance (Fig. 15, p. 35).

REASON FOR ACCOMMODATION

251

Lens At Rest:

eye not adjusted for distance
Lens Moves Backward:

eye adjusted for distance

eye not adjusted for near

Fig. 98 — The 'negative' accommodation of those animals whose eflFort of accommodation
moves the lens backward (lampreys; teleosts; probably holosteans).

Lens At Rest

eye adjusted for distance
Lens Moves Forward:

eye not adjusted for distance

eye adjusted for near

Fig. 99 — ^The 'positive' accommodation of those animals whose effort of accommodation
moves the lens forward (elasmobranchs; amphibians; snakes).

Lens At Rest

eye adjusted for distance
Lens Curvature Sharpens

eye not adjusted for distance

eye adjusted for near

Fig. 100 — The 'positive' accommodation of those animals whose effort of accommodation
sharpens the curvature of the lens (reptiles except snakes; birds; mammals).

252

ADAPTATIONS TO SPACE AND MOTION

There is nothing mystical about this twenty-foot distance. It is that
distance because of the size and structure of the human eye and the
length of human visual cells. This is most important to remember; for
there is a naive tendency for some to assume, on learning that some ani-
mals have no accommodation, that those animals must have hazy images
of all objects nearer to them than twenty feet. This is not true — the
twenty-foot distance is just as much a part of the human eye, and only
of the human eye, as its diameter or its weight.

With Eye At Rest:

With Full Accommodation;

receptive (visual-cell) layer

commencement point is at
infinity, since even parallel
rays focus behiind the retina

(accommodation is used whien object is
anywtiere beyond near point)

near point

tar point is at infinity (parallel rays focus
at /nner surface of receptive layer)

commencement point

(accommodation is used over thus range
of object-positions) — n

c.p.

near point

for point

commencement point

(accommodation is used over this range
of object-positions)|

h-^-H

c.p.

near point

Fig. 101 — Object-positions in relation to accommodation and refractive errors.

The greatest distance at which an object can stand from an eye, and
still be sharply imaged on the retina, is called that eye's 'far point'. Sup-
pose we call by the name 'commencement point' that least distance an
object can have without there being any necessity of accommodation.
For the emmetropic human eye, then, the commencement point — the
point, in the approach of the object, at which the eye must begin to exert
accommodatory effort — is around twenty feet. The hypermetropic or far-
sighted human eye has a much more distant commencement point. Theo-

REASON FOR ACCOMMODATION 253

retically, it lies at infinite distance, for such an eye must accommodate
to some extent to bring even parallel rays (theoretically hailing from in-
finity), let alone rays which diverge ever so slightly, to a focus on the
retina (Fig. 101). The near point of a far-sighted eye is likewise farther
away than that of an emmetropic eye. In myopia the near point is very
close, and the far and commencement points coincide.

But hypermetropia and myopia are abnormalities in human eyes only
because human visual requirements are best met by what we call the 'nor-
mal' condition of emmetropia. We walk and run fast enough to require
sharp vision, without the expense of intraocular muscular exertion, for dis-
tances greater than twenty feet ahead of us. If we habitually travelled
faster — as we are coming to do in this motor age — we should not need
a more distant commencement point, since by relaxing our accommo-
dation we can see sharply as far ahead as the clarity of the atmosphere
allows. But if we habitually crawled on our bellies, we would be much
better off with a closer commencement point, else we should constantly
be exerting accommodation for the distances we most needed to be able
to s^e ahead. Civilized men are so dependent upon clear images of things
which they manipulate with their hands that they need a fairly close near
point. If we were all engravers, we would be better off with a still closer
one — and the 'normal' human eye would be a myopic one.

That the human eye, ideally, is emmetropic is thus a mere coincidence,
and not a sine qua non for all animal eyes. Naturally, there are many
animals with diverse habits which make them need farther or closer com-
mencement points and near points than ours. It is absurd to call their
eyes inferior or disharmonious simply because they do not happen to be
emmetropic.

Devices Which Make Accommodation Unnecessary — We have
seen in earlier chapters that most of the advantages in vision seem to be
on the side of large eyes as against smaller ones. Here, with the matter
of accommodation, the shoe is on the other foot. In a small animal with
small eyes which, ceteris paribus, looks customarily at small objects, the
retinal image not only shifts less laterally when the object moves sidewise
in the opposite direction, but recedes less within the retinal thickness
when the object approaches. Consequently such an eye has a much closer
commencement-point than a large eye — it need not begin to accommo-
date until the object is much nearer. Not only that, but the visual cells
are no smaller in small eyes — just as they are no larger in large eyes,

254 ADAPTATIONS TO SPACE AND MOTION

which the reader will remember as the chief reason why large eyes afford
better-resolved cerebral images (see p. 171). Consequently a small object
can come very close to a small eye before its image recedes off the tips
of the visual cells — as close, perhaps, as the near-point of a large eye
possessing a good mechanism of accommodation. On top of all this, the
small lenses of small eyes have much greater 'depth of focus' than do
the lenses of large eyes; for, the shorter the focal length, the greater the
depth of focus of a lens. The result may well be that the small eye needs
no accommodation at all — so, when we find that the mechanism of
accommodation has undergone phylogenetic atrophy in many small-
eyed nocturnal mammals we are hardly justified in mournfully shaking
our heads at their 'degeneracy'.

In eyes which are large enough to seem to require a capacity for accom-
modation, there are still four ways to dodge the demand and obtain clear
images of objects at various distances, successively or simultaneously,
with a perfectly static intra-ocular situation. All four of these substitutes
for accommodation have been devised and successfully employed by
different vertebrate animals. They are:

1. An increase in the length, or the effective length, of the visual cells.
Vertebrates are strictly limited in the actual lengthening of the receptor
elements, for any such elongation increases the distance between the
inner layers of the retina and an important source of their supplies, the
choriocapillaris. If carried to extremes, this would be detrimental to
retinal nutrition. The cephalopod molluscs with their erect retinae are
under no such handicap, and the visual elements of a squid are so enor-
mously long that the image can recede and advance through their length,
corresponding to great excursions of the object to and from the eye,
without making any demands upon the inefficient apparatus of accom-
modation. Where vertebrates have very long visual cells, as in deep-sea
fishes and some geckoes (see Fig. 25, p. 62), it is of course primarily for
the sake of increasing their sensitivity, though as an incidental effect it
partially obviates accommodation. But in the great fruit-bats, the so-
called flying foxes (Macrochiroptera) , a unique alteration has resulted
in a great increase in the effective length of the rods without these cells
being actually elongated at all: the chorioid is beset with innumerable
conical eminences which deform the visual-cell layer, the elements of the
latter being set endwise against the chorioidal papillae like the trees in a
range of mountains (Fig. 102a). Thus no matter how near or far the
object may be, its image falls sharply upon a set of rods standing at a

DEVICES WHICH OBVIATE ACCOMMODATION

255

corresponding level on the sides of the chorioidal mountains. Presumably
the bat sees the visual field at a given distance as a (relatively!) sharp
reticulum, the lacunae of the lace-work being much more badly blurred.
The small bats (Microchiroptera) do not have this device, but they are
not at all dependent upon their vision, which is very poor; and their eyes
are so tiny anyway as to need no accommodation or substitute therefor.
2. A tilted attitude of the retinal surface relative to the visual axis of
the eye. This is the equivalent of slanting the plate of a camera so as to
have, in simultaneous sharp focus, objects at different distances — as is
done for example in photographing tall buildings from the ground. In
some invertebrate eyes the retina is built like a flight of steps. Among
vertebrates the rays and the horse (and probably many other, unstudied

Fig. 102 — Two devices which make accommodation unnecessary.

a, retina and chorioid of a fruit-bat, Pteropus medius, showing chorioidal mammillation
which places the visual cells at many diflFerent levels, x 48. After Kolmer. x, x- visual-cell
layer, b, eye of a ray, Raja balls, in vertical seaion, showing how retina forms a 'ramp' —
the axial length of the eyeball changes continuously in the vertical meridian. Based on a
drawing of Franz, c, eye of horse in vertical seaion, showing ramp retina. Redrawn from
Nicolas.

ungulates) appear to have produced a similar device, using a ramp rather
than a stairway. The retina is progressively farther from the lens super-
iorly than it is inferiorly (Fig. 102b, c). The horse, which has no power
of accommodation, apparently has only to tilt the eye slightly up or
down to have a sharp retinal image of any object over a considerable
range of distance. This is however only a suspicion which awaits ex-
perimental justification.

3. The use of a stenopaic aperture. This, which is simply a single or
multiple pin-hole pupil or a device which gives the effect of one (as in
the seals — see p. 447), has the virtue of producing a pretty sharp image
regardless of the distances from it to the object and the retina. In fact,
we may fairly say that the vertebrates brought the need of accommoda-
tion upon themselves, in the first place, when they adopted the lens as a

256 ADAPTATIONS TO SPACE AND MOTION

means of forming an image upon the retina, instead of the pinhole as
Nautilus (Fig. Id, p. 3) chose to do. As Figure 89 (p. 224) shows, the
pinhole is a much simpler gadget than the lens, and the image it forms
is quite sharp when caught on a screen at any reasonable distance. But
it has one very great disadvantage: the amount of light, emanating from
an object-point, which can form a corresponding image-point, is just the
slender pencil of rays which get through the pinhole. Apparently, this
pencil should be a single ray if the image is to be maximally sharp, and
the size of the pinhole would then be a quite impractical, mathematical
point.

Actually however, as the pinhole is made smaller and smaller, the
image at first sharpens but finally becomes more and more blurred
through the introduction of diffraction. The optimal diameter of a pin-
hole aperture is equal to twice the square root of the product of the
screen-distance and the wavelength of the light. An ideal pinhole located,
say, at the position of the inner surface of the cornea in a lensless human
eye, would need to be 0.23 millimeters in diameter; and a point four
inches from the eye would then be imaged on the retina as a one-
millimeter circle.

A lens gathers in a cone of light-rays from each point of the object,
and converges all of this light again to form a point in the image, which
is hence far brighter than the one formed by a stenopaic aperture. Other
things being equal, the broader the lens, the brighter the image. Where
a pinhole is employed to eliminate the need for accommodation at cer-
tain times or all the time, the retina must be very sensitive even though
the stenopaic aperture is used in bright light. A reduction of the need
for accommodation — what a photographer would call a deepening of the
focus of the eye — is an incidental gain of any slit-pupilled animal; for a
slit, like a round pinhole, is to be considered a stenopaic aperture, al-
though an astigmatic one. And, slit-pupilled vertebrates always have the
necessary extra sensitivity in their retinae to make vision remain bright
enough when the slit is closed down. That is why they have the slit.

Animals whose pupils are specially designed to provide stenopaic aper-
tures include Scylliorhinus (Fig. 91, p. 225), Ra]a (Fig. 65, p. 158),
geckoes (Fig. 88, p. 223; and see p. 224), some ungulates (especially
camelids — Fig. 86c, p. 219), the domestic cat, and Paradoxurus. Still
others have the benefit of a pinhole in bright light, though their phe-
nomenally contractile circular pupils are no doubt intended primarily to
shield an extra-sensitive retina — a job which ordinarily calls for a slit

PRINCIPAL METHODS OF ACCOMMODATION 257

pupil. These animals are Encheliophis, the sea-snakes, Tarsius, Pedetes,
and the two-toed sloth (see Table VIII, pp. 272-3).

4. The employment of two separate visual mechanisms which are per-
manently set for two particularly useful distances. This method is very
common among the arthropods, where it is expressed in the combination
of compound eyes and simple ocelli as seen in the average insect. Among
the vertebrates, it is used only in the tubular eyes of deep-sea fishes,
whose lenses are relatively so enormous that adjusting them very much
is quite out of the question. Here there is often a second (sometimes
even a third) 'accessory' retina far up the side of the eye, close to the
lens (Fig. 136, p. 400). Distant objects can be seen with this retina while
nearby ones are imaged farther from the lens, on the orthodox retina at
the bottom of the eye. The effect of this arrangement is essentially like
that of the bifocal spectacles to which we resign ourselves in presbyopia.
An even closer approach to a literal bifocal lens is seen in the kingfishers
and particularly in the famous 'four-eyed fish' Anableps, though with
different significances (see pp. 434-5 and 442).

Vertebrate Methods of Accommodation — Few eye-minded verte-
brates have eyes small enough to get along without accommodating, or
have produced one of the four substitute devices described above. The
vast majority alter the optical system dynamically, either by pushing or
pulling the lens backward (Fig. 98) or forward (Fig. 99) — the group
of methods employed by all of the Ichthyopsida (fishes and amphib-
ians); or by changing the shape of the lens (Fig. 100). This may be
accomplished :

A. By squeezing the lens at its equator positively and vigorously by
means of the ciliary body, and with the sphincter of the iris sometimes
called into play to help deform the anterior surface of the lens. This
method is used by all of the Sauropsida (reptiles and birds) except the
snakes, whose ancestors lost the mechanism during their early ocular
degeneracy. The snakes have evolved, as a substitute, a version of the
ichthyopsidan method which is all their own.

B. By relaxing, through muscular effort, a tension which normally
exists (when the muscles are at rest) in the fibers of the suspensory liga-
ment of the lens — thus allowing the elasticity of the lens capsule to mold
the soft lens cortex into a new form with a sharper curvature. This is the
method of the Mammalia (and man) , and differs considerably from the
ancestral sauropsidan one because of the disappearance, in the early mam-
mals, of some structures essential to the complete sauropsidan mechanism.

258

ADAPTATIONS TO SPACE AND MOTION

These three kinds of intra-ocular movements are nearly always accom-
plished entirely by intra-ocular muscles. Extra-ocular ones have been
suspected in some cases of helping to alter the lens-retina distance by
deforming the eyeball in a regular manner. The mechanisms involved
are described below, and are summarized in Table VIII (pp. 272-3),
which should be consulted during the reading of the remainder of this
Section.

?5

Fig. 103 — The eye and surrounding structures in a lamprey, Lampetra fluviatilts, in hori-
zontal section; the anterior end of the animal is to the left. Modified from Franz.

av- anterior surface of vitreous; c- cornea; er- external rectus; io- inferior oblique; ir- internal
rectus; n- optic nerve; s- spectacle (a 'window' in the head skin); sk- skin; sp- space between
speaacle and cornea; sr- superior reaus; /- tendon of cornealis muscle, inserting into spectacle;
V, V- venous sinuses which cushion eyeball.

Lampreys — Inserted into the rim of the primary spectacle (see p. 449/)
at one side is the tendon of a massive muscle (Fig. 103) which lies in the
head outside of the orbital capsule and caudad from the eye, and repre-
sents portions of two myotomes. When this 'musculus cornealis' is con-
tracted, the spectacle is drawn taut and flattens the cornea. Since the
lens touches the latter on the inside, it is pressed backward and nearer
to the retina. The near-point of the resting eye is very close — about five
inches, for the eye is eight diopters myopic. In accommodation the eye
of course becomes emmetropic and may go on into a fairly high degree
of hypermetropia.

Accommodation in the cyclostomes is thus accomplished by deform-
ing the eyeball from outside. The return to the resting shape is effected

ACCOMMODATION IN LAMPREYS

259

through the elasticity of the sclera and vitreous and the equaUty of
intra-ocular pressure throughout the globe. This method is at the mercy
of quick, great changes of hydrostatic pressure and so would not work
well in a fish which makes rapid changes in the depth at which it swims.
Despite the manipulation of the eyeball by the muscle or by water pres-
sure, the lens cannot become dislocated, for it projects well through the
pupil and is firmly held fore and aft by contact with the cornea and the
vitreous (Fig. 103, ay). There is no zonule or suspensory ligament, nor
any need of one, for the spherical lens is trapped like one of the balls
in a ball bearing, the pupil comparing with the aperture in the ball cage
and the cornea and vitreous acting like the outer and inner races.

Fig. lO'l — The elasmobranch eye and its mechanism of accommodation — Carcharodon
carcharius. x 1 1/3 . Combined from figures of Franz.

The eye is represented in full accommodation; were the protraaor lentis muscle relaxed, the
lens would be withdrawn from the cornea, a, horizontal seaion. b, vertical seaion.

c- cornea; ch- chorioid; c{- ciliary folds, from which gelatinous zonule passes to lens equator;

ext- external rectus; i- iris; inf- inferior rectus; int- internal rectus; /- lens; op- optic pedicel;

p- papilla bearing protractor lentis muscle; r- retina; s- suspensory 'ligament' (a thickening in

the zonule); sc- scleral cartilage; sf- fibrous portion of sclera; so- superior oblique;

sup- superior rectus.

The musculus cornealis does not interfere with the rotation of the
eyeball, as it would do if inserted into the true cornea instead of into the
primary spectacle. There is obviously some reason to think that the con-
version of the spectacle into a conjunctiva (see Chapter 11, section D)
had to wait for the evolution of intra-ocular muscles of accommodation.
It has been claimed that the lamprey's oculomotor muscles (which are
very thin and much blended where they cling to the globe, and reach far
forward so as to form a smooth jacket) accomplish accommodation for
near objects by contracting in unison and thus elongating the eyeball.
There is as yet no adequate experimental basis for this belief, and

260 ADAPTATIONS TO SPACE AND MOTION

there would seem to be no need whatever for such an action since the
resting eye is too long (that is, myopic) to begin with. Such an action
of the external muscles might however serve to combat any temporary
flattening effect of water pressure in lampreys which descend to consid-
erable depths, as ocean species are known to do.

Elasmobranchs — In the elasmobranchs the lens is again spherical or
nearly so (Fig. 104). The iris does not commence at the ora terminalis
as in lampreys, for a ciliary body with many low radial folds intervenes.
A washer-shaped, gelatinous membrane, attached peripherally over the
whole surface of the ciliary body and centrally around a narrow equator-
ial zone on the lens surface, serves as a zonule. A dorsal, radial thicken-
ing in this membrane gives the lens most of its actual support. Diametri-
cally opposite, in the ventral meridian, there is an elaborate papilla on
the ciliary body which contains smooth muscle fibers. These fibers are so
oriented that when they contract, they swing the lens pendulum-fashion
toward the cornea. Accommodatory effort is thus exerted for near vision,
as in ourselves, and not for distant vision as in lampreys and teleosts. The
anterior chamber is very shallow, but there is always some space between
the relaxed lens and the cornea. The depth of this space represents the
range of accommodatory movement of which the lens is capable — unless,
as may be, the little protractor lentis muscle is strong enough to make the
lens bulge the cornea somewhat. The eyes of elasmobranchs have con-
siderable hypermetropia — ten to fifteen diopters in various species,
according to Franz; but they can accommodate from fifteen to twenty
diopters, hence may have very close near points.

Teleosts — Teleost fishes have a mechanism which is superficially similar
to that of the elasmobranchs but actually can have no evolutionary con-
nection therewith. Here again the lens is spherical, and touches the cornea
as in the lampreys (Fig. 105). It is suspended by a dorso-nasal ligament
consisting of material essentially like tough vitreous, and running from
the pars caeca retinae to the surface of the lens a little anterior to its
equator. On this ligament the lens can swing — not freely as an undamped
pendulum however, since there is evidence for the presence of a diaphan-
ous zonule with radial and even circular fibers, anchoring the lens to the
pars caeca in all meridians.

Approximately diametrically opposite the suspensory ligament, but
with much variation in location and structure from species to species,
is the tendinous insertion, in front of the lens equator, of a small ecto-

Fig. 105 — The teleost eye and its accommodation.

In each drawing (except e), the temporal side of the eye is on the left, the nasal on the right.

a, generalized teleost eye in horizontal optical section. After Franz, av- anterior surface of
vitreous; c- cornea (cf. Fig. 67, p. 159, for detailed labelling of its three portions) ; eg- chorioid
'gland'; cm- ciliary muscle (tensor chorioideee' ) ; fp- falciform process; x- iris; /- lens; on-
optic nerve; re- retina; rl- retraaor lentis muscle; sc- scleral cartilage; so- scleral ossicle
(cf. Fig. 130b, p. 380); vc- vitreous cleft; z- zonule, b, left eye of Blennius sanguinolentts
from above, in relaxation, x 3. After Beer, c, same as b; in full accommodation; note
temporad duction of lens accompanying retraaion. d, the adjustment of a teleost eye for
an approaching object (relaxation of the retractor muscle, and return of lens forward to its
rest position); o-o'-o"- successive positions of objea; l-l'-l"- successive positions of relaxing
lens; i-i'-i"- successive locations of retinal image, in the absence of a fovea which would call
for fixative rotation of the eye. e, cross seaion of optic nerve of Serranus cabrilla, showing
edgewise-folded ribbon structure characteristic of many teleosts. From Franz, after Studnicka.
f, eye of Serranus cabrilla in relaxation, showing anterior aphakic space common in teleosts
and often associated with a fovea temporalis. Modified from Beer, g, diagrammatic frontal
section of teleost eye, showing mechanism of accommodation. Based on a figure of Meader,
/- embryonic fissure; /- lens; n- motor nerve in falciform process; r- retraaor lentis muscle;
s- suspensory ligament.

261

262 ADAPTATIONS TO SPACE AND MOTION

dermal retractor lentis muscle, sometimes called the 'campanula (or
plumula) Halleri', The other tendon of this muscle originates tem-
porally and cranially in the anterior end of the falciform (= sickle-
shaped) process where such is present. The falciform process is a
ridge in the floor of the eyeball, running from behind and temporally
(near, at, or even from above the disc) forward and nasally along more
or less of the length of the original course of the embryonic fissure of
the optic cup (see Chapter 5, section A) , The falciform process may be
most simply (though not too accurately) described as a herniation of
the chorioid up through the unclosed fissure. It is lacking in many fishes
without much regard to their taxonomic positions, and its place in the
internal nutritional system of the eye is always taken by a system of
('hyaloid') blood vessels spread out in a thin membrane at the vitreo-
retinal interface. In fishes which lack the falciform process, the lens-
muscle is kept but its fixed anchorage punctures the retina near the ora.

The nasoventral attachment of the lens-muscle, and its orientation,
result in a backward (craniad) and temporad duction of the lens upon
contraction. The impulses to contraction come over a large branch
of the oculomotor nerve which runs along through the chorioid be-
neath the falciform process and, accompanied by a blood vessel, de-
parts from the process anteriorly and runs free through the ocular cavity
to reach the little muscle. The movement of the lens is roughly opposite
to that accomplished in the elasmobranch eye by the protractor lentis,
and accommodates the teleost eye for distance instead of for near.

Except in the tubular eyes of many deep-sea teleosts (whose lenses
can only be moved slightly backward, if at all) , the lens moves laterally,
toward the fish's tail, rather more than it moves backward into the retinal
cup. This is particularly true in species which have a fovea (see p. 304).
During accommodation, a teleost's attention is obviously upon the image
in the temporad periphery, which is the location of the area centralis and
is the part of the retina involved in binocular vision.

The retractor lentis muscle in its various manifestations undoubtedly
does all of the actual work of accommodation in the teleost eye. How-
ever, in this group a ciliary muscle is first seen. It is so very small that
it makes no bulge in the ciliary region of the uveal tract; and, there being
no ciliary folds (except a few dorsal and ventral ones in a few species, as
also in the rays among the elasmobranchs) there is really no discrete
ciliary body at all. The uvea is much alike from ora terminalis to pupil
(Fig. 67, p. 159), and unless one calls this whole region 'iris' one must

ACCOMMODATION IN FISHES 263

define the latter rather arbitrarily as 'the portion of the anterior uvea
which is visible through the cornea', in order to distinguish the remain-
der as a ciliary body.

The ciliary muscle fibers run from the inner surface of the rim of the
cornea to the outer surface of the chorioid at or near the ora terminalis,
and because of this disposition were long called a 'tensor chorioideae'
muscle, and were believed to tauten the chorioid around the vitreous to
maintain turgidity and an unvarying optical situation during the move-
ments of the lens. The chorioid is too firmly plastered onto the sclera
anteriorly to make the need of such an action plausible, however, and at
present we are helpless to explain the teleostean ciliary muscle as any-
thing but a phylogenetically precocious, 'orimentary' or pre-adaptive
structure, of unknown but minor importance, which very conveniently
hung on until the reptiles found an important job for it.

By and large, teleosts are more or less myopic — up to as much as 15
diopters, the highly abnormal telescope gold-fish even more so. This is
to be expected, since approaching the lens to the retina would only put
their eyes out of focus for any and all distances if they were not myopic
to start with. Their eyes are thus set for close work with a minimum of
effort, and they need to exert muscular force only when attending to
distant objects — and 'distant', for the average fish in the average natural
body of water, means only up to fifty feet at most. Beyond this distance
underwater vision — anything more than light-sense — is practically nil.
Many mud-grubbing, small-eyed fishes are hypermetropic, indicating a
loss of importance of vision to them, for which we will see an exact
analogy among the mammals (v. i.) .

Other Fishes — Of these we can say little. Nothing is known concern-
ing accommodation in the living cladistians, Polypterus and Calamoich-
thys. Nothing whatever is known as yet concerning the eye of the newest
'living fossil', the crossopterygian Latimeria cbalumnae.

Dipnoans appear to have no accommodation. In the small-eyed forms,
at least, there is no ciliary body, no zonule, no lens-muscle. In Lepido-
siren and Protopterus this is comprehensible, for the whole eye, and par-
ticularly the retina, is so very crudely built as to make accommodation
a useless refinement. The relatively large eye of Neoceratodus deserves
further study. This lungfish does not aestivate in mud, and spends much
of its time at the surface of the water (see Fig. 61a, p. 137), where its
eyes should be quite useful.

264 ADAPTATIONS TO SPACE AND MOTION

The 'ganoids', too, need more attention. Hess was unable to detect
any accommodatory changes in the sturgeon. The eyes of the spoonbills
(Polyodon and Psepburus) have not been studied from any standpoint,
to say nothing of accommodation. In the holosteans (Amia, Lepisos-
teus), there is an ectodermal lens-muscle, but it is not known whether
it is homologous with that of the elasmobranchs or with that of the
teleosts; nor is it even certain whether it pulls the lens forward, or back-
ward and sidewise.

Matt hies sen's Ratio — The optics of the fish eye — of whatever tax-
onomic category — was exhaustively studied years ago by Matthiessen.
This worker found that the fish eye is more thoroughly standardized
than any other. The refractive index of the lens nearly always varies
parabolically from 1.51 at the center to 1.38 (as in mammals) at the
surface, giving it a higher effective index (1.649—1.653) than that of
any other vertebrate type. The lens is a sphere, and the optical properties
of the other media are constant, the indices of the humors low (about
equal to water — 1.33+), so that the difference between lens- and humor-
indices is maximal. Thus the fish eye should always have the same pro-
portions regardless of its size — and indeed Matthiessen found close
agreement to exist between the theoretical and the actual. The distance
from lens center to retina, for instance, should ideally be 2.55 times the
radius of the lens, and it rarely actually differs from this figure, known
as Matthiessen's ratio, by more than one or two integers in the last deci-
mal place — even in the tubular eyes of deep-sea forms, which were once
called telescopic because they were thought to be radically different from
ordinary fish eyes in their optical principles.

Optical Elimination of the Cornea — The conformation of the fish
cornea is of no consequence whatever, since its refractive index is so near
to that of water that it has no focusing power. It is not surprising to find
that the piscine corneal epithelium is often irregular in thickness, the
cornea sometimes having concentric ridges and the like which would be
fatal to clear vision in a land animal. All responsibility for image-for-
mation rests on the lens, which, for the sake of periscopy, must lie against
the cornea and even project from the level of the head surface if this is
feasible. This necessity has kept the fishes using their ancient methods of
accommodation; for until, in land animals, the cornea came to share in
refraction, thus allowing the lens to be drawn back farther into the eye,

ACCOMMODATION IN FISHES 265

there was no way in which pressure could be conveniently brought to
bear upon the equator of the lens to change the radii of curvature of its
surfaces.

Consequences of Lens Movement — The very fact that the fish lens
is never required to change its shape affords one advantage, however, for
the lens is enabled to be firm and thus to have a relatively high index of
refraction — reaching, in one silurid, a value of 1.72+, which is rather
higher than that of most optical glass. The axis of the fish eyeball can
consequently be its shortest diameter, thus economizing a bit upon
space in the head. But the shiftings of the lens during accommodation
introduce a complication whose existence is often neglected : the aqueous
humor being incompressible, the lens can move only if the aqueous is free
to get out of its way. In the lampreys, the deformation of the globe in
accommodation results in no actual change in volume of the anterior
chamber, for the lens remains always in contact with the cornea. In the
teleosts, when the lens is drawn backward by the retractor lentis, the
aqueous in the posterior chamber is free to flow through the pupil, if need
be, to keep internal pressures balanced. But in the elasmobranchs the for-
ward movement of the accommodating lens tends to seal off the anterior
chamber by pressing the lens against the pupil margin, for there is no
canal of Schlemm. These fishes have consequently had to leave unclosed
a small portion of the embryonic fissure, at the root of the iris, so that the
aqueous can flow readily between the anterior and posterior chambers.

Amphibians — The amphibians are not completely emancipated from
the water, and a few frogs and salamanders never leave that medium for
a moment; but the eyes of amphibious amphibians have undergone whole-
sale modification, for vision through air, both as regards the structure of
the globe and the production of protective adnexa. The cornea comes
into its own here as the principal refracting structure, the lens becoming
merely adjuvant to the accommodatory adjustment of the location of the
image. The anterior chamber is deepened by the regular dome-shape
taken on by the cornea, so that the eyeball is practically spherical (Fig.
106) ; and the lens lies much deeper in the eye than in fishes, since it no
longer needs to protrude through the pupil. Closer responsiveness of the
iris to the intensity of illumination is thus permitted, and the photome-
chanical changes of the retina here begin their phylogenetic degeneration
(see Table II, p. 150).

266

ADAPTATIONS TO SPACE AND MOTION

The entrance of the cornea into the optical picture, together with the
elongation of the axis of the eyeball, has permitted the lens to flatten
somewhat in land forms. The ratio of its equatorial and axial diameters
is aroimd 1.3 : 1 instead of 1 : 1 as in fishes and aquatic salamanders. The
lens does not owe this slight flattening to tension in the zonule as in our-

Fig. 106 — The amphibian eye and its accommodation.

a, anuran eye in vertical seaion. x 11/4. Based largely on Rand pipiens.

ac- area centralis (marked by local concentration of visual cells) ; io- inferior oblique; ir- in-
ferior rectus; //-lower lid; /rn, /m- lens muscles (protractors); «- optic nerve; «wz- niaitating
membrane (transparent, independently movable portion of lower lid — not homologous with
sauropsidan and mammalian nictitans); pn, pn- pupillary nodules (urodeles have only the
ventral one, and only the ventral lens muscle); sc- scleral cartilage; so- superior oblique;
ST- superior rectus; «/- upper lid; z- zonule (fibers are embedded in vitreous) .

b, anterior segment of Bufo sp., in relaxation, x 3, From Franz, after Beer.

c, same as b; in accommodation; note forward movement of lens.

selves, however; for, despite the fact that the amphibian lens is in such a
position that it might be changed in shape, it is rather firm and is changed
only in position, for accommodatory purposes, just as in all fishes.

The amphibian mechanism of accommodation is a close imitation of
that of the elasmobranchs; but the muscles involved are mesodermal

ACCOMMODATION IN AMPHIBIANS 267

ones, rather than ectodermal. The amphibian zonule is more distinctly
fibrous than that in lower forms, but is not so well extricated from the
vitreous. Vitreous substance fills that space* between the radial zonule
fibers which, in a mammalian eye, would be an aqueous-filled 'canal of
Hannover' with its contents communicating freely with those of the pos-
terior chamber (see p. 19). There is scarcely any ciliary body — it is just
wide enough to form an attachment for the peripherally converged fibers
of the zonule. The more-or-less radial 'ciliary folds' of frogs are really
iris folds on the back face of that organ, Mid-ventrally however there is
one heavy fold which deserves to be called a ciliary process, and it is to
this that the ventral (in salamanders, the only) protractor lentis muscle
inserts, running from its origin at the sclerocorneal junction through the
root of the iris. The protractors are thus not connected directly to the
lens, but their pull is communicated to it by the ciliary 'processes' and
the bundles of zonule fibers attached thereto.

The delicate zonule fibers fan out to the equatorial zone of the lens
from the neighborhood of the annular hyaloid vessel which lies on the
minute ciliary body. Since the site of origin of the fibers is so narrow, the
lens can move forward and backward without much hindrance from them.

Unlike the elasmobranchs which also pull the lens forward, the
anurans have a canal of Schlemm, though a discontinuous one consisting
of a dorsal and a ventral crescent. Accommodation is too rapid, however,
to afford time for aqueous to escape from in front of the advancing lens
by diffusing into the canal, and there is no convenient open slit through
the iris root mid-ventrally, for this slit (see p. 265) has been occupied by
the ventral protractor lentis muscle. Hence the urodeles (which lack the
canal) have produced a nodule of hard connective tissue at the mid-ven-
tral point of the pupil margin, which lifts the iris free of the lens capsule
locally, and allows the aqueous to flow around to the back of the lens as
the latter moves forward. Anurans ordinarily have a dorsal pupillary
nodule as well (Fig. 106a, pn), corresponding to a second, dorsal, pro-
tractor lentis muscle. The ciliary muscle is no better developed in am-
phibians than in teleosts, and is no more obviously useful in any way.

Newts are emmetropic under water; and in the air, where the cornea
comes into optical play, they would become very strongly myopic. Frogs
are emmetropic in air. Under water, they of course become strongly
hypermetropic, and are quite unable to compensate therefor with their
limited range of forward lens-movement. No amphibian has as much as
five diopters of accommodation, and many apparently have none at all

268 ADAPTATIONS TO SPACE AND MOTION

— particularly the most secretive forms with the most active pupils,
whose crude eyes mediate mere light-sense rather than form-sense (e. g.,
Megalobatrachus japonicus) . The refraction of toads has not been much
studied; but land forms might be expected to be emmetropic or myopic
in the air, and hypermetropic when in the water during the breeding
season. Toad rods are longer than frog rods, helping to reduce the need
for accommodation, though toads (Fig. 106b, c) do have more accommo-
dation than frogs anyway. Salamandra is known to be emmetropic in air.

Role of the Vitreous in Ichthyopsidan Accommodation — The

vitreous humor is an important part of the mechanism of accommodation
in the Ichthyopsida, although this is not at first apparent. The original
vertebrate eye did not at first possess any semblance of a zonule, and
without the jellification of the mass of fluid lying behind the lens, the
latter could not be held in place icf. Fig. 103, p. 258). In the vertebrate-
like eye of a squid (Fig. Ig, p. 3), where the tough 'epithelial body'
serves as a zonule, the Vitreous cavity' behind this lens-holding plate of
tissue is filled with watery liquid, not with a jelly. In the lampreys, the
elastic cushion of the vitreous keeps the lens propped against the cornea
and insures that the position of the resting lens will always be the same
at every relaxation of accommodation.

In the elasmobranchs the gelatinous, discoid zonule, though far less
strong than the tissue 'zonule' of a cephalopod, might perhaps restore
the lens to position after relaxation of the protractor lentis, even if the
vitreous were not jelled. In the teleosts, however, the elasticity of the
vitreous is needed to serve as a quick-acting antagonist of the retractor
lentis, which must work against it and could not single-handedly replace
the lens simply by elongating in relaxation.

According to this idea, the vitreous — or at least its gel condition — is
ordinarily a useless vestige in the higher vertebrates and has only per-
sisted because (being transparent) it does not interfere, and affects
nothing but the distribution of accommodatory deformation between the
anterior and posterior lens surfaces. It returns to usefulness however in
the snakes, and in those few amphibious reptiles, birds, and mammals
which squeeze the front of the lens with the sphincter iridis, tending to
force the lens backward. This tendency must be controlled by the cush-
ioning action of the vitreous, and by the zonule fibers acting as check
ligaments; else in these animals, the efforts of the iris to increase the
refracting power of the lens would be nullified by a decrease in the
distance from lens to retina.

SAUROPSIDAN MUSCLES OF ACCOMMODATION 269

Sauropsidan Muscles of Accommodation — ^With the advent of the
Sauropsida the eye underwent a considerable revolution, especially as
regards the mechanism of accommodation. None of the great changes
involved is even hinted at, in any extant amphibians, and their production
therefore cannot be traced. In the reptiles, pro- and retractor lentis mus-
cles are finally abandoned, though a new mesodermal lens-moving mus-
cle, the transversalis, makes its appearance in turtles and lizards and is
concerned with swinging the lens sidewise in the eye, toward the nose,
thus aiding in the convergence of the two visual axes for the purposes of
binocular vision (Fig. Ill, p. 278).

The sauropsidan method of accommodation involves an actual periph-
eral squeezing of the lens, the power coming from a ciliary muscle which,
compared with the puny one in the Ichthyopsida, is massive indeed. The
whole ciliary body is conspicuous and elaborate. Its muscle fibers, and
those of the iris as well, differ greatly from those of fishes and amphib-
ians in that they are of the striated type, histologically, instead of smooth.
How profound a difference this may make physiologically, we do not
really know. Striated muscle elsewhere in the body differs from smooth
muscle in being ordinarily voluntary, in having no inherent rhythm of
contraction, in greater rapidity of action, and in its propensity for easy
fatigue. But the smooth muscles of vertebrate eyes are not quite like
those of the rest of the body. The dilatator iridis is not a fully-differenti-
ated muscle at all, though it and the sphincter iridis are physiologically
and pharmacologically indistinguishable (despite their ectodermal origin)
from somatic smooth muscles or from the ciliary muscle, which has more
in common with somatic muscles embryologically. Human accommo-
dation is notoriously fatigable, this being the usual basis of 'eyestrain';
but whether the residence of the fatigue is the muscle itself, we do not
know.

We hardly know what to expect from the striated sauropsidan homo-
logues of these contractile structures. Would they, like the striated
muscle of the heart, contract rhythmically if denervated? This has not
been tested. Are they voluntary? The iridic muscles of birds certainly
seem to be — but so do the smooth-muscled irides of a few mammals. Are
they unusually fatigable as compared with the corresponding mammalian
muscles? Of this, we know nothing.

If any one of the usual differences between smooth and striated mus-
cles does exist here, to serve as a 'reason' for the change, it would seem
to be the greater rapidity of contraction of striated muscle. If striated

270

ADAPTATIONS TO SPACE AND MOTION

intra-ocular muscles were known only in the birds, we would be ready to
argue that they had been developed for rapidity of action, without wait-
ing for experimental proof — for common sense would tell us that the
fast-flying birds must need extra-rapid accommodation. The situation in
the birds' only vertebrate competitors, the swift fruit-bats, seems corrobo-
rative; for it is easy to say that the reason why the Macrochiroptera have
given up all efforts to accommodate, and have produced the substitutive
retinal deformation described above, is because the early mammals inheri-
ted only slow-acting, smooth intra-ocular muscles from their particular
reptilian ancestors (see Fig. 60, p. 135) — or else had returned their
ciliary muscles to an unstriated condition before the bats evolved.
But what need have the plodding reptiles for any ultra-rapid accom-

Fig. 107 — Scleral ossicles in sauropsidans. After Edinger.

a, ossicular ring of Sphenodon punctatus, with '+' and '-' ossicles designated, xl'/i.

b, skull of an eagle, Aquila chrysa'etos, with ossicular ring in place, x %. c, single ossicle
of A. chrysa'etos. x 1. d, eyeball of albatross, Diomedea regia, showing how ossicles sup-
port the concavity of the corneoscleral junction, x % . b- bursalis muscle; c- cornea; er-
external rectus; n- optic nerve; or- ossicular ring; so- superior oblique; sr- superior rectus.

modatory capacity? Many lizards, of course, are remarkably agile — and
of all land reptiles the lizards have the most extensive and rapid accom-
modation. But this is most marked in the chameleon, than which no ver-
tebrate (unless it be the sloth) moves more slowly — except for its light-
ning-like tongue. The answer is that these and other lizards are insectivor-
ous: they need rapid accommodation as much because of the speed of
their prey as because of their own rapidity of movement. And even a
turtle has been seen to strike and grasp a grasshopper in flight.

Scleral Ossicles in Sauropsida — The sauropsidan sclera typically
consists largely of a cartilaginous cup whose open rim extends quite close
to the limbus of the cornea. Just as typically the remaining zone of the
sclera is occupied by a circlet of thin overlapping plates of bone, the
scleral ossicles (Fig. 107). These are lacking only in crocodilians and

SCLERAL OSSICLES OF SAUROPSIDANS

271

snakes — the latter also lacking the scleral cartilage, among a great many
other ocular structures which other sauropsidans possess. The scleral
ossicles are not convexly curved to continue the rotundity of the equator-
ial sclera smoothly into the sharper curvature of the cornea. On the con-
trary they are flat or even concave, so that the whole zone of the sclero-
corneal junction is depressed or concave to form a broad annular sulcus
(Fig. 107d). This sulcus is important to the fundamental processes of
sauropsidan accommodation. The ossicles which are responsible for it are
therefore considered here as a part of the mechanism of accommodation
in these vertebrates.

There is little question as to the evolutionary source of these ossicles,
but the time of their origin is in doubt. Surrounding the eyes of fishes is
a ring of small skull bones, the circumorbitals. The overlying skin often
bears a sense organ (of the lateral line system) centered over each of the

Fig. 108 — Sauropsidan embryos,
showing sensilloid papilla at pe-
riphery of cornea: evidence for
the origin of scleral ossicles from
extra-ocular bones (see text).
From Franz, after Dabelow.

a, Lacerta agilis. b, Vanellus sp.

circumorbital bones. In sauropsidan embryos the scleral ossicles arise as
dermal bones which sink into the sclera, and the ectoderm over each one
temporarily shows a sensilloid papilla (Fig. 108). It thus appears that
the scleral ossicles are homologous with the originally ex/rd-ocular cir-
cum-orbital bones.

Another theory derives the sauropsidan scleral ossicles from the scleral
bones of fishes, which being co-existent with the circumorbital bones could
scarcely be homologous with the latter. Ancient armored fishes had four
plates in the anterior sclera, forming a closed ring. Modern fishes show
at most only two of these — if they are indeed homologues. In some swift
swimmers, the tuna and swordfish for example, the two plates are joined
to make a complete ring and are protective against the impact and dis-
tortive pressure of the water (see Fig, 130, p. 380),

These oligomeric ossicular rings of fishes have been dubiously homo-
logized with the polymeric ones of the Sauropsida through two question-

TA BL E 3mi-

LENS MOVED
FORWARD BY:

BACKWARD BY:

LENS POWER
INCREASED BY:

CO

UJ

I

Ll

Lampreys

elasticity of eyeball

extra-ocular
(cornealis) muscle

Elasmobranchs

ventral, ectodermal
protractor muscle

relaxation

Holosteans

?

?

Teleosts

relaxation

ventral, ectodermal
retractor muscle
(ropid-octing in littoral
SDD..such as blennies)

Al! others

1

Anurans

dorsal a ventral, meso-
dermal protractors

relaxation

Urodeles

ventral, mesodermal
protractor muscle

relaxation

CcEcilians

if)

LU
_l

1—
CL
UJ

Sphenodon

Ciliary

(Brucke's)

muscle

Crocodilians

Turtles

Lizards

ciliary (Crompton's,
BrucKe's) muscles

Snakes

mesodermal muscle
in ins root presses ir-
is against vitreous, a
indents sclera; vitre-
ous, under pressure,
pushes lens forward

relaxation

Dupil sphincter, in
amphibious spp.

if)

Q

m

Terrestrial spp.

Brucke's a Cramp-
on's muscles-, may
3lso be a Muller's

«

Amphibious spp.

Brucke's (Cramp-
on's lacking); circ -
jiar fibers in M?ri7S

—I
<

<I

Most

Aquatic

Sea-
cows

Whales

2^ !
o ^

^^
-"c

Ij toothed: Brucke's,
5 may be Muller's;
jboleendittle or no
ijciliary muscle

Amphi-
bious

e.g.
otters

'.Brucke's (a Mull-
yer'sT) muscle(S)

Seals

1 Brucke's
^ and
3 Muller's
\ muscles

Primates

Man

Others

'Not the same 'Muller's muscle' as that of mammals; see text.

272

MECHANISMS OF ACCOMMODATION

EXTENT OF
ACCOMMODATION

ACCESSORIES i^
SUBSTITUTES

REFRACTION*

REMARKS

oculomotor muscles
antagonize corneal?

8D >8D

[Lampetra fluviatilis)

stenopoic pupis m
rays a Scyliiorhinus

+I0-I5D

I5-20D

slit at ins root allows
transfer of aqueous

lens-muscle present,
function not known

small ciliary muscle,
function not known

OS much OS -I5D
(in water) in good-
eyed 'i^^AAnabas,
OP in air)

probably ordinarily
enough 1o overcome

tne myopia
[Anabass\o accomm.)

ste

nopaic pup.
Encheliophi.

c pupil in

IS

prob no ace (unless
in Neoceratodus)

strictly aquatic spp.
OD in water-, amphib-
ious a terrestrial spp.
probably all OD in air

never >5D (never e
nough to abolish the
hypermetropia of a
land sp. under water)

pupillary nodules al-
low aqueous transfer

probably have.no
gccomrnodation

sphincter of iris
aids considerably

OD,or nearly so, in air;
strongly + in water

nocturnal, but ossicles
retained (has a fovea!)

probably never >2D

nocturnal — ossicles
have been discarded

stenopaic pupils
in most geckoes

marine spp.OD in wo
ter. all others OD in air

more than enough to
give emmetropio in i-izO

OD

great

less ace. in marine a
strictly terrestrial spp.

Crompton's muscle
may 'sharpen' cornea

pupil becomes
stenopaic in

sea-snakes, when
out of water

+ 2-9D

0-17D

muscle of accomm.
in iris derived from
Brucke's muscle

>muscle cells in
chorioid
'focus' 'fove'cE

Pf'n\^°P|(^/0/e^/??s myopic)

great

Crompton's muscle
increases focusing
power of cornea

sphincter of ins
usually aids; often
'lens' in nictitans

(penguins are — inairl

very great
) (cormorants: 40-50 D)

kingfishers: a unique
occommodation-ob
viotinq device (tex

stenopaic pupils, romp
retinae, in some (see
text); fruit-bat retina

as much as +1D
(very small eyes, high +)

usually little or none,
but may be up to4D

[Dugong)-^[) in air,
■ Strongly + in water

Brucke's muscle may
be present, but with
no apparent function

apparently none

no ciliary muscle

unknown

toothed: presumably
considerable; baleen:
not more than 1/2-ID

very powerful iris
sphincier aids greatly

OD

more than enough to
give emmetropio in HzG

in air, pupil is a slit, a
cancels astigmatism

high myopia^. a c
neal astigmatism in
air, nullified by slit pupil

enough to restore
emmetropio in water

astigmatism elimin-
ated when under H20

true normal +'/2D(?)

about 10 Dot age 21

highly variable (like
domesticated spp.)

stenopaic pupil
Tarsius

'D,or OS high os+ID
.boPoons ore myopic)

not >IOD

^D=diopters; +=hypermetropia; — = myopia; 0 (zero)=emmet ropia

273

274 ADAPTATIONS TO SPACE AND MOTION

able links : an imaginative reconstruction of one extinct crossopterygian
fish which postulates a polymeric ring, and the situation in the extinct
amphibians (the Stegocephali) .

Irregular bits of bone occur in the sclera of Triturus pyrrhogaster, and
the Brazilian frog Stereocyclops (=Hypopachus) incrassatus has an
ossified annulus around the cornea; but in no modern amphibian can any
certain counterparts of the sauropsidan ring be found. The stegoce-
phalians, however, had 'scleral ossicles'. These usually numbered 20-32
and were set in several rows. Moreover, they almost always formed only
a dorsal half -moon — rarely a closed and single ring. These bones may
have been homologues of the piscine circumorbitals, but it is much more
likely that they formed a sort of mail on the upper lid and were thus a
part of the head armor which was characteristic of the group and indeed
gave it its very name. And even if they were indeed in the sclera, they
could not have been involved in accommodation, for they formed only
part of a circle.

The whole mechanism of accommodation which we are here calling
'sauropsidan' — including the scleral ossicles — may really have been in-
vented by the stegocephalians, which were certainly diurnal and may
have had sufficiently acute vision to make an excellent accommodation
worth while. But if so, the right stegocephalian for showing the origin
of the ossicular ring has not yet been found fossil. It may be significant
that of the cotylosaurs, the stem-group of the reptiles, no specimen has
yet turned up showing scleral ossicles.

The scleral bones number sixteen or seventeen in Sphenodon. They
were lacking in Pleurosaurus, the largest aquatic rhynchocephalian rela-
tive of Sphenodon, thus affording an interesting comparison with the
modern crocodilians in which the ossicles probably disappeared upon the
advent of nocturnality, with its crude images and consequent uselessness
of accommodation. The Mesozoic marine crocodiles had them — at least
in the sidewise-looking Metriorhynchidae and in Pelagosaurus, the one
member of the Telosauridae whose eyes were not directed upward.

Modern reptiles and birds have fourteen plates more often than other
numbers. Fourteen are usual for lizards, though there may be as many
as sixteen or as few (Chamaleo) as eleven. Turtles have still lower num-
bers— Konig found from six to nine in Testudo grceca, ten in Emys
orbicularis. Birds have up to eighteen, the passerines having fourteen.
Phylogenetic schemes based upon ossicular numbers have been attempt-
ed, but unsuccessfully.

ACCOMMODATION IN SAUROPSIDA

275

The bones may be so dovetailed into each other that the ring is im-
mobile (Fig. 107b, c), or they may so overlap that they can slide on one
another; but there is no experimental evidence that they ever do so.
'Plus' and 'minus' plates are distinguished as to whether they overlap
both of their neighbors or are overlapped by both, and these exceptional
plates tend to occur in the vertical or the horizontal meridians, or both
(Fig. 107a), There is always an unusual situation mid-ventrally (where
either a '+' or '— ' plate or an edge-to-edge junction without overlap
occurs) — attributed to the disturbance of the formation of the plates
created by the embryonic fissure of the optic cup.

THIS SIDE,
RELAXATION

THIS SIDE,
ACCOMMODATION

Fig. 109 — Diagram of generalized reptilian mechanism of accommodation.

ap- annular pad of lens; bm- Briicke's muscle; bp- base plate of ciliary body; c- cornea;
ch- chorioid; cp- ciliary process; i- iris; lb- lens body; ot- ora terminalis; pi- pertinate liga-
ment; /, /- sclera; sc- scleral cartilage; scs- sclerocorneal sulcus; so- scleral ossicle; sr- sensory
retina; tbm- tendon of Briicke's muscle (continuous with inner layers of corneal substantia
propria); //- tenacular ligament; z- zonule.

Accommodation in Sauropsida (Except Snakes) — The produc-
tion of a sulcus is the whole meaning, physiologically, of the sauropsidan
ossicular ring. It stiffens the concavity against the force of the intra-
ocular pressure which, if unresisted, would evaginate it. This pressure
rises slightly during accommodation, which it does not do in fishes,
amphibians, or mammals. On examining a sagittal section of a saur-
opsidan eye we see the internal result of the sclero-corneal sulcus: an
approximation of the ciliary body to the lens.

276 ADAPTATIONS TO SPACE AND MOTION

This is further aided by two other devices, the ciUary processes and
the 'Ringwulst', or 'annular pad' (Fig. 109). CiUary processes are to
be sharply distinguished from ciliary folds. The latter may be radial
or circular and are always low affairs whose significance is solely the
increase of the secretory or absorptive surface of the thin layer of blind
retinal tissue which covers them, the ciliary epithelium. The folds on the
posterior surface of the amphibian iris (there being no room for them
on the narrow ciliary body) are in the same category.

Ciliary processes differ morphologically from ciliary folds only in a
quantitative way, but they have a separate physiological significance.
They are tall, fin-like structures (Fig. 110) and serve to bring the
ciliary body into firm contact with the lens, with which (in Saurop-
sida) their tips are actually fused. The ciliary body, if it lacked them,
might still be made to reach to the lens equator and contact the annular
pad smoothly all the way around. But, there would be two difficulties
about such an arrangement. The more grave one would be that the
retrolental space would be sealed off from the posterior chamber so that
aqueous could not transfer back and forth between the two during
accommodation, as it is free to do between ciliary processes. Also, the
ciliary body would tend to be 'muscle-bound', with a great deal more
internal friction during the action of its muscles, if its constrictive force
were not transferred indirectly to the lens through the ciliary processes.
If one imagines the spaces between the processes to be filled in with
solid material, one can see that as the ciliary zone decreased in diameter,
this material would have to be compressed; and the energy required for
this useless compression would be lost from the effective action of the
ciliary muscle upon the lens. Only the lizards have been able somehow
to reduce the size of the processes almost to the vanishing point and still
employ the standard sauropsidan method of accommodation. They may
have some difference in the mechanics or hydraulics of the phenomenon
which accounts for their heresy.

While the scleral ossicles and the ciliary processes extend the ciliary
body axiad to meet the lens, the latter comes half-way, so to say, by its
production of the annular pad. In Sauropsida, after the ordinary circum-
ferential lens fibers have been laid down, the lens epithelium in the
equatorial region does not remain simply cuboidal or columnar. Its
cells elongate enormously, without swinging their axes through 90 to
become ordinary circumferential lens fibers (compare Fig. 109, ap, with
Fig. 41a, p. 111). The result is an equatorial thickening on the lens,

ACCOMMODATION IN SAUROPSIDA

277

whose elements are radially disposed and thus admirably oriented for
their service as architectural columns, transmitting the radial stress of
the ciliary processes directly to the spherical heart of the lens. Thd
annular pad has no optical function whatever, for the iris shields it
and the image-forming light beam is confined to the more onion-like
nuclear portion of the lens. Like the softness of the lens in Sauropsida,
the thickness of the annular pad, as might be expected, goes with activity

Fig. 110 — Anterior segment of left eye of a turtle {Emys orbicularis'), seen from behind,
showing junction of ciliary processes with lens capsule (characteristic of sauropsidans — con-
trast Fig. 44, p. 115). X 13. After Konig.

/- unclosed portion of embryonic fissure; /- lens; o- orbiculus ciliaris; p- ciliary processes;

r- sensory retina.

of the ciliary muscles, in its variation from species to species. It is thick-
est of all in the chameleons.

The ciliary muscles in birds and lizards have the same location as
those of non-lacertilian reptiles, but are more complicated, as is explained
below. The fibers of sauropsidan ciliary muscles are all meridional except
in a very few species, and have their origin in the inner layers of the
cornea at its margin. Their insertions are not into the chorioid, as in the
Ichthyopsida, but are scattered along the orbiculus ciliaris much as in the

278 ADAPTATIONS TO SPACE AND MOTION

mammals. There is often a tenacular ligament (tl in Figs. 109, 112)
running from the sclera to the orbiculus just in front of the ora termi-
nalis, which prevents the chorioid's being drawn forward. Thus when
the ciliary muscle contracts, it can have but two possible actions —
and only the first of these unless the sclerocorneal sulcus happens to be
quite well marked: (a) a stretching of the orbiculus and a heaving of the
corona of ciliary processes forward and toward the axis of the eye, thus
pressing them against the lens. Any actual forward movement of the lens
is checked partly by the weak suspensory-ligament fibers, partly by the
'pectinate ligament' running from cornea to iris root across the angle
of the anterior chamber (Fig. 109, pi). The force of contraction of die
ciliary muscle is thus largely diverted to the accomplishment of an
actual squeezing of the lens, (b) A traction backward and axiad upon

Fig. Ill— Transversalis muscle of a lizard, Lacerta serpa, as seen in a frontal section
through the region (mid-ventral) of the embryonic fissure. After Lasker.

c- connective tissue of ciliary body; /- unclosed portion of embryonic fissure; m- transversalis
muscle; r, r- pars ciliaris retina; t- tendon of muscle, which inserts on lens.

the limbus corneas, deepening the sclero-corneal sulcus and sharpening
the curvature of the cornea.

How much of the latter action {b) ever occurs in reptiles is a question.
It would be helpful in accommodating the eye for near objects; but most
of the accommodation is certainly brought about by the sharpening of
the anterior curvature of the lens. The posterior surface of the lens abuts
upon the relatively unyielding vitreous, and the periphery of the anterior
surface against the similarly firm iris root. Hence most of the defor-
mation of the lens is confined to a central area on the anterior surface —
just as it is, by an utterly different mechanism, in the human eye (see
Fig. 109, p. 275; cj. pp. 32-4 and Fig. 14, p. 31).

It used to be thought that a deformation of the sclero-corneal region,
impressing the vitreous and causing the latter to push the lens forward,
was the chief or only factor in sauropsidan accommodation. Ingenious
experiments made a few years ago by Hess, however, have shown that the

ACCOMMODATION IN BIRDS 279

general processes described above are what actually take place. Hess
proved that there is no increased pressure on the vitreous, by showing
that in an excised eye the process will occur quite normally under elec-
trical stimulation, even though the posterior half of the eyeball be cut
away.

Even though the lens does not move forward very far, it bulges for-
ward and encroaches upon the anterior chamber. The birds (except the
nocturnal ones) have left patent that same meridional, ventral slit in the
anterior uvea which we remarked in the elasmobranchs, to permit the
equalization of anterior and posterior chamber pressures. Despite this
provision, the aqueous pressure rises a little as noted above. In lizards
and turtles, the transversalis muscle runs through an homologous
aperture (Fig. Ill; see Fig. 110, /).

The details of the accommodatory process in the crocodilians (which
have no scleral ossicles) remain to be worked out. The group has had
less attention than others, perhaps because material is hard to obtain in
Europe. Our abundant alligator is going begging for want of a curious
American physiologist. All that is known is that it does accommodate,
though very slightly and slowly. The beast is emmetropic, or a diopter
or so hypermetropic, in air. Under water, it must be 15-20 diopters of
more hypermetropic.

Special Features in Birds and Lizards — The accommodating equip-
ment of birds differs from that of reptiles only in minor respects. The
transversalis muscle (never, apparently, concerned with accommodation
so much as with binocular vision) has been found only in the pigeon. It
may not be an homologue of the reptilian one, but rather an aberrant
slip of the ciliary muscle itself.

The birds share with the lizards one muscle, Crampton's, which is
unique but is clearly a derivative of the ordinary reptilian ciliary muscle.
The reptilian ciliary, which is a husky descendant of the little ichthyop-
sidan tensor chorioidese, runs from the corneal margin and the inner sur-
face of the anterior sclera to the base-plate of the orbiculus ciliaris. The
situation in the birds is as if this reptilian ciliary muscle had been cut in
two all the way around the eye, half-way back along its course, the two
halves then being stretched enough to let the cut ends overlap (Fig. 112).
Crampton's muscle represents the corneal end of the reptile ciliary. Near
its posterior, inner surface is seen the insertion of a second (Briicke's)
muscle which continues backward toward the ora terminalis. Briicke's

280

ADAPTATIONS TO SPACE AND MOTION

muscle thus represents the posterior portion of the ancestral reptilian
ciliary. Briicke's name is often applied to the whole of the ciliary in forms
below the birds, as well as to the radial or meridional portion of the
mammalian ciliary muscle where this has given rise (as in primates) to a

/cm-.

.pl/CP^

~-bm

op

^bp

ch.

-of

Fig. 112 — The accommodatory apparatus of birds. Semi-diagrammatic;
based upon the situation in the hawks.

ap- annular pad of lens; bm- Briicke's muscle; bp- base plate of ciliary body; c- cornea;
ch- chorioid; cm- Crampton's muscle (entirely intrascleral ) ; co- conjunctiva; cp- ciliary pro-
cess; i- iris; lb- lens body; ot- ora terminalis; pi- pectinate ligament; s, s- sclera; sc- scleral
cartilage; so- scleral ossicle; so'- overlapped portion of adjacent scleral ossicle; sr- sensory
retina; tcm- tendon of Crampton's muscle (continuous with inner layers of corneal sub-
stantia propria); tl- tenacular ligament; z- zonule.

circular 'muscle of Miiller'. Quite another 'Miiller's muscle' occurs in
some birds, where it is simply the posterior portion of a further-sub-
divided Crampton's muscle, with its fibers still radial in orientation. In
lizards, Crampton's muscle is even more distinct from Briicke's than it is

ACCOMMODATION IN BIRDS 281

in birds, for it is completely embedded in the sclera. Brucke's muscle
inserts, not upon Crampton's, but upon a partition of scleral material.

The anatomical and physiological divorce of the anterior part of the
ciliary muscle from the posterior, together with the especially deep sclero-
corneal sulcus of birds, seems designed to promote the cornea-deforming
action which we noted was possibly present, though not marked, in rep-
tiles. At least, it is in the birds which have the heaviest Crampton's
muscles (hawks and owls) that the cornea changes most in shape during
accommodation. Again, in diving birds, whose corneae are extra-thick
and stiff, and of no optical use under water anyway, Crampton's muscle
is all but absent.

Another, and little-understood, muscular apparatus of bird eyes which
may have something to do with accommodation is found in the fundal
portion of the chorioid. Here (particularly, it is claimed, in the neigh-
borhood of the fovea) there are scattered short, thick muscle cells run-
ning rivet-fashion through the thickness of the chorioid. It has been
suggested that these, by varying the thickness of the chorioid, serve to
adjust very precisely the position of the fovea in accommodation. Their
action would be comparable to that of the fine adjustment of a micro-
scope, the ciliary muscles being the coarse adjustment. It is as likely that
they regulate the blood volume of the chorioid and thus affect vitreous-
cavity volume and pressure during accommodatory changes or changes
in altitude during flight. In some birds these chorioidal muscle elements
are striated, in others smooth, in still others absent; and until these dif-
ferences have been studied further and correlated with other avian fea-
tures, intra-ocular or extra-ocular, we will have no certainty as to quite
what they mean. If they are indeed a micrometer adjustment for accom-
modation, they may explain why avian foveal cones are not elongated, as
are those of other foveate animals in which such elongation relieves the
accommodation of the necessity of being extremely precise (see p. 182).

Most birds are emmetropic or a little hypermetropic, but the wingless
kiwi (Apteryx) is somewhat myopic. This nocturnal bird is reputed to
have poor vision at all distances, especially in the daytime; and it un-
questionably has the poorest eye, all-round, of any bird. As would be
expected, diurnal birds have somewhat more extensive accommodation
than any reptiles, the extent of accommodation being related to their
feeding habits (see p. 366). Even such ordinary-eyed birds as the domes-
tic hen and pigeon have a range of eight to twelve diopters; but the owls
have half of this or less. The homer, whose vision is probably better than

282 ADAPTATIONS TO SPACE AND MOTION

that of any other breed of pigeon, has been found experimentally to
have a near-point at 40 centimeters. This implies that there is a consider-
able hypermetropia in the resting eye.

Snakes — Turning to the snakes, we find that all sauropsidan rules are
off. As is explained fully in Chapter 16, the snakes seem to have origi-
nated as animals whose way of life was such as to allow the eye to degen-
erate extensively. Among the parts lost from the equipment handed on
to them by their good-eyed lacertilian ancestors were such items as scleral
cartilage, scleral ossicles, ciliary processes, annular pad, and (the eye
being very badly off indeed for a time!) iris muscles. In modem snakes,
the sclera is fibrous as in higher mammals, the eyeball consequently
spherical.

The snakes eventually had to make good all of these losses as best they
could. The ciliary body being far out of contact with the lens, and with
its proper musculature stolen by the iris to become a revamped pupillo-
motor apparatus, it is quite out of the picture of accommodation. The
only intra-ocular muscles are the mesodermal ones of the iris, which have
been taken into the iris secondarily from the ciliary body. These muscles,
along with their new job of operating the pupillary aperture, have had to
retain the function of accommodation which they had when they were in
the ciliary body, but perform that function in an entirely new way :

The iris is pressed forward into a strongly conical shape by the spher-
ical lens (Fig. 154, p. 456). At its root there is a powerful aggregation of
sphinctral fibers — those which have moved least from their old position in
the ciliary body. When these fibers contract, they draw in the sclero-
corneal junction and put a pressure upon the vitreous which it in turn
communicates to the back of the lens. The main body of the sphincter,
near the pupil, and the more-or-less radially disposed iris fibers also
contract simultaneously. The conical iris tries to flatten back into a
plane, augmenting the backward pressure upon the vitreous. The end
result is that the firm lens moves bodily forward, without appreciable
change in shape, a third to a half of the distance from its resting position
to the cornea. The cornea may also move forward a little, due to an
elongation of the eyeball which compensates for a reduction in its equa-
torial diameter by the pull of the iris. Accommodation in the snake eye
is thus accomplished essentially as in the eye of the squid (in which,
likewise, the intra-ocular pressure is raised in accommodation), and re-
sembles that of only the elasmobranchs and amphibians among the
vertebrates; and even there only to the extent that the lens is fixed in

ACCOMMODATION IN SNAKES 283

shape (water snakes excepted) and moves forward, adjusting the eye for
nearer objects. The physiological indentation of the anterior scleral re-
gion is so pronounced that the sclera may even have a couple of perma-
nent meridional furrows anteriorly, in readiness for their further deep-
ening during accommodation.

Beer found that in a snake eye in which the posterior sclera had been
cut away, and in which the accommodatory action was evoked electri-
cally, the lens moved backT^ard. This was due to the (unbalanced) rise
of anterior-chamber pressure, which in the intact eye is far exceeded by
the rise in vitreous pressure, so that the lens has to move forward. Ac-
cording to Beer, various snakes are anywhere up to nine diopters hyper-
metropic, but most have more than enough accommodation to overcome
their refractive error.

In some snakes, particularly those with a fovea {Dryophis and The-
lotornis) , there is a nasad component of the forward motion of the lens.
This is exactly equivalent, in its optical consequences, to the nasad move-
ment of the lens of a teleost when the accommodation is relaxed to adjust
for near objects. The same basis obtains in the two cases: a strongly
temporal position of the area centralis in the retina (see Fig. 79, p. 186;
cj. Fig. 77, p. 185, and Fig. 105d, p. 261).

Mammals — As with peoples and their governments, vertebrate eyes get
the kind of accommodation they deserve. The degree of 'eye-mindedness'
in the subphylum sinks from the higher jfishes to the amphibians, rises
sharply in the reptiles, still higher to a peak in the birds and falls off
woefully again in the mammals — with some recovery in the highest forms
and a very considerable one in the squirrels and simians, to be sure. The
engineering efficiency of the accommodatory apparatus runs exactly par-
allel with this variation in the value set upon vision.

The mammals originated as small-bodied, small-eyed, forms which
were almost certainly nocturnal. Within the marsupial and placental
series, parallel evolution has culminated in the production of swift, large-
bodied, large-eyed types (the kangaroos on the one hand, the ungulates
on the other) , adapted to open country, where good vision is more valu-
able than to a forest animal. Such animals have expanded their visual
capacities to twenty-four-hour performance and some have gone on close
to diurnality, with a steady increase in visual acuity. The more eye-
minded forms, with much sharper vision than their primitive relatives,
may also have much more extensive accommodation. But since their
evolution passed through the bottle-neck of the monotremes, opossums.

284 ADAPTATIONS TO SPACE AND MOTION

and insectivores (see Fig. 60, p. 135), they have had to get along with
whatever portions of the beautiful sauropsidan mechanism those antique
nocturnal mammals happened to retain.

That was not much, for aside from the ciliary muscle itself — and this
has retrograded to the unstriated type — not one of the sauropsidan
adjuncts to vigorous accommodation remains in any mammal. Though a
slight circumcorneal sulcus (marked in apes and man) may be present,
it is not an indentation of the sclera itself and is never supported by
scleral ossicles; nor is there ever an annular pad on the lens. The mono-
tremes have a vestige of the pad and have kept the scleral cartilage, thus
presenting a tunica fibrosa which is matched in the sauropsida only in
the crocodiles — likewise nocturnal and primitive within their class. In no
mammal are the ciliary processes joined to the lens capsule, and in only
a few are they ever even in light contact with it during accommodation.
This simplification of the mammalian eye, giving it an essentially
amphibioid make-up, has led one prominent phyleticist (Franz) to
suggest that the placental mammals were derived from forms intermedi-
ate between the amphibians and the reptiles, with only the monotremes
and marsupials (the former having scleral cartilage, and both groups
showing double cones and oil-droplets in their retinae) tracing back to
fully differentiated reptiles.

The comparative anatomy and palaeontology of the occipital condyles
would seem to make such a diphyletic origin of the mammals quite im-
possible. The placental mammals lack so many of the sauropsidan ocular
structures, not because their ancestors never had them, but because the
small-eyed sub-insectivores were so strictly nocturnal that they discarded
these daytime features as so much excess baggage. The oldest known
mammals averaged less than rat-sized and are indicated, by their den-
tition, to have been insectivorous and granivorous. Wherever among the
placental mammals very small size has reappeared, even the inferior
mammalian mechanism has failed to evolve, or has been allowed to
disappear.

The most important result of the wholesale discardments of reptilian
ocular structures in the mammals has been to take the ciliary body out
of intimate contact with the lens — especially far out, in the simians and
the echidnas, despite the breadth of their lenses. Those semi-diurnal and
diurnal mammals which have rebuilt an effective accommodation have
consequently (like the snakes) been under the necessity of developing
a brand-new method.

ACCOMMODATION IN MAMMALS 285

This method, seen at its best in man (see Chapter 2, section B) , makes
use of the elasticity of the lens capsule to furnish the actual force of
accommodation. The contraction of the ciliary muscle, by easing the
tension in the fibers of the zonule which normally hold the lens flat-
tened, merely releases this elastic force and lets it go to work. In some
amphibious mammals, as in the turtles, water-snakes, and diving birds,
the sphincter iridis comes into play also to aid in accommodation (Chap-
ter 11, section C). Even in these mammals, the ciliary muscle still
apparently does most of the work, for it is more massive than in strictly
terrestrial species.

Their employment of capsule elasticity is probably wholly original
with the mammals. The elasticity is not a useful factor in sauropsidan
accommodation which can be regarded as having been simply exagger-
ated by the mammals. Reptilian lenses do take on something like their
accommodated shape, when they are cut free from their attachments.
But the zonule fibers are probably not under greater tension in the rest-
ing eye than in the accommodating one, as they are in mammals. More
likely their tension increases in accommodation, since they apparently
serve as check-ligaments rather than as the real supports of the lens.

Among the land mammals, the ciliary muscle is well developed only
in ungulates, carnivores, and primates. It is seldom so compact as in man.
More often there is much connective tissue between the fibers, so that
although the muscle is bulky, it is not strong. In many small, large-lensed
mammals (e.g., mice) it consists of but a few fibers, or is even entirely
lacking. Even where it can be made out easily, as in domestic ungulates,
it may accomplish nothing because of the great size of the lens and the
relative weakness of the capsule. The horse, sheep, and pig have no
accommodation, and such instances serve to emphasize that though the
ciliary muscle may propose, it is the elasticity of the lens capsule which
disposes — just as in a presbyopic human being.

Circular ciliary muscle fibers, forming a 'muscle of Miiller' with an
especially efficient orientation (see p. 33), are known to occur only in
seals, primates (best in man) and in some toothed whales and some
ungulates. This distribution is important to remember; for every so often
someone comes along with experiments based upon pharmacological
responses, which 'prove' that the radial and circular portions of the
ciliary muscle in mammals are antagonists, the circular fibers adjusting
the eye for near and the radial ones, just as actively, for distance. Such

286 ADAPTATIONS TO SPACE AND MOTION

work, it will be found, is always done upon cats or perhaps rabbits —
neither of which has any circular fibers whatever.

The whole ciliary body may be so oriented as to put the ciliary muscle
at an advantage or at a decided disadvantage, because of great inter-
specific variations in the shape of the mammalian eyeball which in turn
are due to considerations which happen to be more important to the eyes
concerned than accommodation. Thus in the prosimians the ciliary body
may be tubular like the eye itself (Fig. 84b, p. 213), while in sirenians
and whales it may lie in a plane continuing that of the iris (Fig. 140b,
p. 409; Fig. 141a, p. 413).

Like the vitreous humor, the ciliary processes in the terrestrial
mammals and man are functionless vestiges so far as mechanical impor-
tance is concerned. Any such importance disappeared as soon as the pro-
cesses lost their former approximation to the lens, for the accomplishment
of which the reptiles evolved the processes themselves, the scleral ossicles,
and the annular pad. They do serve as convenient attachments for some
of the zonule fibers, but would seem not to be indispensable in this con-
nection. They have persisted presumably because, as with ciliary folds
and iris folds, their great contribution to the aqueous-secretory surface
is valuable for the regulation of the intra-ocular pressure. Franz sharply
distinguishes between two types of processes in different species: a
rugose, vascular kind (e.g., man — see Fig. 6c, p. 14) and a thin, rel-
atively avascular kind (e.g., cat). The meaning of these differences is
not surely known, but they imply a difference in secretory capacity.

According to Lindsay Johnson, wild mammals normally show a slight
hypermetropia (up to one diopter) , which is better for animals which do
no close work with hands than myopia would be. Myopia is normal only
for mandrills and other baboons, which is comprehensible considering
that these are the only sub-human primates which have abandoned the
trees for a life on open ground, where food objects are smaller. A little
hypermetropia is even better than emmetropia for most mammals of any
size, for two reasons : (a) because with increasing age the lens hardens
and its index of refraction rises, making an emmetropic eye become
somewhat myopic as time goes on. An initial hypermetropia will delay
this change to a greater age of the animal, by allowing 'slack' for the rise
in refractive power before that rise results in a myopia; and (b) because
since a hypermetropic eye must accommodate a little even at long object-
distances, the tonus of the accommodatory muscles is always fully devel-
oped and the apparatus is alert for the performance of any needed

ACCOMMODATION IN MAMMALS 287

change of setting. If an eye is one diopter hypermetropic, it needs only
one diopter of accommodation in order to make itself emmetropic, and
thus obtain sharp images all the way to the horizon. And with only two
diopters of accommodation, it can give itself a near-point at one meter —
ordinarily quite close enough, for any animal that cannot read!

Among zoo animals and domesticated ones, just as with auto-domesti-
cated— i.e., 'civilized' — man, anything may happen. In fact, it is wholly
unsafe to draw ecological conclusions from any situation in domestic
species. Less than fifty per cent of horses are emmetropic; and though
myopia is most unusual for a wild mammal, it is extremely common in
zoo animals and barnyard varieties.

Along with their normal slight hypermetropia, ungulates usually show
a slight horizontal astigmatism, probably a consequence of their efforts to
widen the visual field horizontally by every possible means (see pp. 299-
300). The extent of accommodation is very low indeed in mammals —
often zero — except in the primates. The cat, which is the nearest com-
petitor of the simians in this regard, has but half the accommodation of
a thirty-year-old man and loses even this in old age. Human accommo-
dation being 'tops' for mammals (Beer found no more than ten diopters
in any ape), it is desirable to turn back to the graph (Fig. 15, p. 35)
showing its extent at various ages. The senescent diminution of the
power of accommodation in mammals is bound up with the accommo-
datory method itself. Certainly in the Ichthyopsida no such falling-off
is to be expected, for the lens in these animals may become even harder
with age than it is in the young, without this affecting the range of
accommodation a particle. In the Sauropsida, the direct action of the
ciliary muscle probably accomplishes an effective alteration of lens form
at ages where, if the animal were a mammal of the same relative age,
the lesser force of the elasticity of the lens capsule could no longer make
headway against the sclerosis of the lens fibers.

A special situation arises in small-eyed mammals. The squirrels are
exceptional among the rodents, in having some accommodation, which
we should expect from their diurnality and high visual acuity. The Eu-
ropean squirrel may be emmetropic or as much as one-half diopter hyper-
metropic, and can accommodate from one to one and one-half diopters.
As the size of the eye diminishes from that of a cat to that of a mouse
(Fig. 71, p. 173), the increasing (relative) size and firmness of the lens
and its (relative) recession toward the retina results not only in the
reduction of accommodation from a couple of diopters to nothing, but

288 ADAPTATIONS TO SPACE AND MOTION

also in an increase of the hypermetropia from a half-diopter or so to
five, seven, even ten diopters. This situation has been branded as a dis-
harmony, supposedly inevitable in small eyes simply because they are
small. This notion ignores the optical perfection of even smaller fish
eyes. The apparent disharmony simply reflects the indifference of mice
and mouse-sized mammals in general to any refinements of vision relat-
ing to resolving power. The cerebral images of mice and the like are so
crude at best, that the eye is useful more for recording the intensity and
direction of light, and the motion of large objects in the visual field,
than for discrimination of pattern. In such animals, the 'nose knows'
far more about the environment than does the eye.

(B) Visual Angles and Fields

In all vertebrates, vision predominates in any accurate localization of
objects in space. Aside from vision, only audition and olfaction are
telassthetic senses — that is, capable of giving information about objects
and events at a distance. The distance and direction of an object which
is beyond arm's reach can be only crudely judged by these other tel-
aesthetic modalities, and can be accurately evaluated only through vision
if at all. Audition is notoriously untrustworthy as a means of localization.
The finding of an object by olfaction is a trial-and-error process, and is
not localization at all in the sense of a pre-knowledge of location.

The visual registration of space entails the embracement, by the retinae,
of light rays coming from many directions. The animal may be thought
of as having its head at the center of a sphere of space. The proportion
of that sphere within which the animal can see is influenced by several
factors :

A. The visual angle, in various meridians, of each eye;

B. The position of the eyes in the head and the ratio of binoc-
ular field to total visual field;

C. The orientation of the visual axes, where these do not coin-
cide with the anatomical optic axes;

D. The capacity for reflex and voluntary eye movements and
the location of the area centralis or fovea, if one is present;

E. The capacity for head movements in compensation for any
severe reduction of visual angle or eye mobility.

VISUAL ANGLES AND FIELDS 289

Visual Angles — The angle — or rather, cone — of space subtended by
the retina is surprisingly uniform throughout the vertebrates. It is rarely
much greater or much less than 170°. This angle is influenced by the
angular extent of the retina. If the functional retina comes far forward
in the eyeball, as in the horse, the eye may see through an angle much
greater than 180°. If the tissue is restricted to the fundus of a tubular
eye like that of the owl, the visual angle may be as little as 110°, and
is still smaller in deep-sea fishes.

The visual angle is affected also by the cornea, though not in a way
which is self-evident. If the projected area of the cornea in the plane of
the limbus be divided into the area of the retina, a quotient is obtained
which one might suppose to represent the visual angle. This quotient has
been found to be 13.5 for man, 11.5 for a falcon, 10.4 in the pigeon,
4.0 in an owl, only 2.5 in a bat. The visual angles of these eyes do not
bear such numerical relationships to each other. The cornea-retina quo-
tient expresses rather the concentration of light upon the retina and
affects the sensitivity of the eye, not its visual angle. If, however, we
consider the angular size of a cornea — the portion it includes on a sphere
of its own curvature — we have a better indication of the angle of space
which that cornea will place upon the retina behind it — provided the
retina's own angular size is great enough to receive all of it, which is
not always true as for instance in the owls. The human cornea subtends
only 60 of a circle with its own radius, and is relatively small. That of
the cat occupies 107°. A single human eye sees through 150°, a cat eye
through 200 . The bending of the light rays as they pass through the
cornea accounts for the apparent discrepancy of the visual angle (which
is the effective angular extent of the retina) and the angular size of the
cornea. Where the angular size of the retina exceeds that called for by
the properties of the cornea, obviously the anteriormost part of the retina
must be non-functional. This is true, for example, of the human retina in
a zone which extends backward for three millimeters from the ora termi-
nalis. This zone is blind, and is said to contain no rhodopsin.

A very special case is that of the chameleon, whose thick circular lid,
fused to the cornea, leaves a crater-like opening the size of the immobile
pupil, through which the eye has only 'tube vision' with the whole periph-
ery of the retina unable to receive light. One might wonder why the
chameleons have not pared away this useless peripheral portion of their
eyes as the owls have done. Perhaps it is because they have needed to
retain the hemispherical shape of the back of the eyeball to enable it to

290 ADAPTATIONS TO SPACE AND MOTION

roll smoothly in the orbit during their extensive eye-movements. Ordin-
arily, the eyelids impose no restriction upon the visual angle of the eye.
We can look up and see our eyebrows, which means that they are con-
cealing a part of space from us; but we cannot see our lid margins, even
as unfocused shadows.

Another special case is that of the fish. The cornea having the same
refractive index as the water, it is optically eliminated. The lens then
takes over the control of the visual angle; but, being spherical, it imposes
no limitation at all and the visual angle is thus determined in the last
analysis by the angular extent of the retina. The strongly refractive fish
lens usually protrudes from the level of the surface of the head, and is
oftentimes able to place much more than 180° of space upon much less
than 180° of retina (Fig. 128, p. 376) — at least in the horizontal plane,
where an aphakic space often helps out considerably.

Position of the Eyes in the Head — Many a careless writer has stated
that phylogenetically, 'from fish to man', there has been a gradual migra-
tion of the eyes from a position back-to-back to one in which the two
lines of sight are forward and parallel. Actually, a complete series of eye
positions can be arranged wholly within the fish group, another such
series within the birds, and a third within the mammals. Scattered species
elsewhere have the lines of sight parallel, but directed upward rather than
forward. The development of a frontal position of the eye from an initial
lateral one has taken place several times independently. Some cases of
'frontality', as for example in deep-sea fishes (see Fig. 138, p. 403) have
rather special interpretations. But by and large one finds a good
correlation with predacity: the hunters tend toward frontality so as to
have the best vision of the prey they are pursuing, while the hunted tend
to retain laterality of eye position so as to be able to detect an enemy
coming from any direction. The predaceous animal can afford not to
have such 'eyes in the back of his head', because his offensive weapons,
teeth and claws, give him immunity from stealthy attack. Carnivores
rarely make a habit of feeding upon other carnivores, for the risks are
too great and the meat is too tough.

The most important effect of variations in the positions of the eyes
is to vary the extent of the binocular field and the direction in which it
lies — usually forward, but sometimes more or less upward. The binocular
visual field is simply the spatial cone or zone within which the separate
monocular fields overlap. Its value to the animal and the character of

VISUAL ANGLES AND FIELDS 291

vision within it will be disaxssed in detail farther on. Suffice it to say at
this point that two eyes are better than one, and that vertebrates in gen-
eral have seemingly striven to enlarge their binocular fields at the ex-
pense of their uniocular ones (uniocular being used here to denote the
part of a monocular field which is not overlapped by that of the other
eye). Animals which have clung to strong laterality have done so in
obedience to powerful factors, such as defenselessness (e.g., rabbits) or
total absence of cover in the environment (e.g., pelagic fishes), which
make the retention of periscopy vitally important. The various degrees
of partial frontality are compromises between the urge for binocularity
and the need for periscopy.

In most groups of vertebrates the predaceous habit is a very common
specialization; so, the associated tendency toward frontality is likewise
common. Remembering that the visual field of a single eye is roughly
constant at 170 or so, we may consider the angular width of the binoc-
ular field to be quite directly related to the angle between the two optic
axes, which in itself will depend upon the position of the eyes in the head.

Extent of the Binocular Field — There are very few vertebrates in-
deed which are known for certain to have no binocular field whatever.
The lampreys, the hammerhead sharks and a few large-headed teleosts,
such chunky amphibians as Cryptobranchus, the penguins of the genus
Spheniscus, and the larger whales constitute these exceptions. In some
other animals, as the chameleons and probably some fishes, there is no
binocularity when the eyes are at rest but it can be created by convergent
eye movements. Wherever the eyes are mobile, there exists the theoretical
possibihty of widening the binocular field by convergence of the optic
axes; but as we shall see, this possibility has been realized only in forms
which have developed an area centralis with or without a fovea, for only
such forms have any ability to move the eyes at will.

The extents of the static binocular and uniocular fields have been
estimated for many animals by different means at various times. Over
a century ago, the positions of the eyes of a great number of vertebrates
were judged by Johannes Miiller from the angle between the planes of
the two orbital rims. Miiller assumed the optic axes to be perpendicular
to these planes. In 1877, Grossman and Mayerhausen also published a
long list of figures, based upon the divergence of the axes of the two
corneae. In modern times these patient researches have had to be dis-
carded, for the optic axis is neither normal to the plane of the orbit

292 ADAPTATIONS TO SPACE AND MOTION

margin nor necessarily coincident with, or even close to, the visual axis
— the actual physiological line of sight in fixation (cf. Figs. 3, 16;
pp. 7, 37).

Paradoxically, the optic axis can be considered to be the visual axis
only when there really is no visual axis — that is, where there is no area
of acute vision or fovea and hence no fixation or precise aiming of the
eye at objects. In mammals there is usually an area, but it is central
(except in ungulates) and here the orientation of the optic axis does
become a fair criterion of the direction and extent of the binocular visual
field. Lindsay Johnson's chart of mammalian inter-axial angles (Fig.
113, p. 297) is therefore acceptable; but a similar chart for fishes (whose
foveae are strongly temporal) would be worthless as indicating the direc-
tion of best vision with the eyes at rest.

The best studies have been the recent ones of Rochon-Duvigneaud,
Kahmann, and Pisa, who have made direct determinations of the visual
fields by observing the trans-scleral images of a movable light, in dis-
sected heads clamped in a perimeter. Most of our accurate knowledge
of visual fields in animals has come from these investigations.

In fishes, Kahmann found that the binocular field measured usually
from 20 to 30 in the horizontal plane. There were wider variations
among the marine forms, where the angle might be as small as 4 (Box,
Trigla) or greater than 30 (Trachurus, Cepola, Serranus, certain
labrids, and especially in flatfishes) . Among freshwater forms the widest
binocular fields, and thus the greatest degree of frontality, were in such
predators as the trout, perch, and pike, with values ranging from 30°
to 40 or more. But on the marine side the predaceous Julis revealed a
value of only 15° and the mackerel-like Lichia, 8°. A great surprise to
Kahmann was the low value of 14 for the archer-fish, Toxotes jaculator
— which, by analogy with the snakes which have the habit of striking
and hence have similar visual requirements, might be expected to have
as wide a field as Dryophis (v./.). One fish, Chlorophthalmus agassizH,
probably does rival Dryophis, for it is reported to have a strikingly
similar pupil (see Fig. 79, p. 186). In one type of chondrostean, the
spoonbill or paddlefish Polyodon spathula, the eyes are aimed forward
about as frankly as in some deep-sea fishes (see Fig. 138b, p. 403). But
since they are set on the dorsal side of the 'paddle' near its base, their
view downward is cut off.

Because of their periscopy, nearly all fishes also have something of a
dorsal binocular field. Bottom-dwelling fishes have truly specialized such

VISUAL ANGLES AND FIELDS 293

a field, and it amounts to 25° in some star-gazers (genus Uranoscopus) ,
30-40 in some of the blennies, and to still higher values in other star-
gazers (Astroscopus*), in many batoids and flatfishes, and in such for-
ward-and-upward-lookers as the toadfish, Opsanus tau. Purely accidental
and of little value on the other hand, is the narrow posterior binocular
field which many fishes possess. The nasal retina is too crude for them
to make any real use of such a field. A ventral or downward binocular
field is useful to pelagic fishes, and some surface forms (needlefishes,
halfbeaks, flyingfishes, the look-down [Vomer setipinnis] etc.) have their
eyes canted downward to produce one; but in most fishes the angle
between the optic axes in the vertical plane is concave upward.

Amphibians nearly all have a binocular field, wider in anurans than in
urodeles and much reduced or absent in some of the latter; but no exact
determinations appear to be on record. The horizontally oval pupil of
most frogs and toads would tend to extend the binocular field a bit, but
its primary meaning is probably in connection with periscopy.

The reptiles show less variation than the fishes (see Table IX,
next page). The crocodilians have about 25° of binocular field. In the
turtles, one extreme is given by the herbivorous Testudo (18°), and the
other by the snapping turtle, Chelydra (38 ). Two-thirds of the snap-
per's food is animal, and half of this consists of game fishes. The snap-
ping turtle strikes its prey like a snake, and thus has special need of the
good distance-judgment which binocularity confers. The lizards have the
strongest laterality of the eyes, with binocular fields of only 10 to 20
as a rule. Though most species are predaceous their prey is small; but the
lizards themselves have much to fear from predaceous birds and mam-
mals, and have therefore retained their periscopy. The monitors (Varan-
idae) are big enough to fear nothing, however, and anticipate their sup-
posed descendants, the snakes, with values of 30 or more. In snakes the
binocular angle ranges mostly between 30 and 40 , with higher values
in strongly eye-minded, striking snakes such as Dryophis, whose key-hole
pupil is a clever device for widening the binocular field without this being
(as it is in Zamenis flagelliformis) at the expense of periscopy. The river-
snakes, Acrocbordus javanicus and Cerberus rbyncbops, have an exten-
sive binocular field which is directed largely upward, but these forms
seem not to be guided by vision at all. Kahmann states that they 'tongue'

*The species of Astroscopus stare fixedly upward. In this genus the eye-muscles are much
reduced, and portions of one or more of them have been converted into a huge electric
organ, occupying the enlarged orbit in which the small eye has been crowded forward.

Table IX

VISUAL FIELDS IN REPTILES (After Kahmann, rearranged)

Groups and species

Turtles

Chelodina longicollis

Testudo ibera

Geomyda trijuga

Clemmys caspica

Chelydra serpentina

Crocodilians
A Hi gat or mississippiensis. . .

Caiman niger

Caiman sclerops

Lizards

Trachysaurus rugosus

A nguis fragilis

Tiliqua nigrolutea

Lacerta viridis

Iguana tuber culata

Physignathus lesueuri

Ophisaurus apus

Chalcides ocellatus

Basiliscus plumifrons

Z.onurus giganteus

Varanus griseus

Snakes

Trimeresurus wagleri 141

Chrysopelea ornata 136

Leptophis liocercus 131

Python molurus 137

Coluber longissimus

Coluber leopardinus 165

Tarbophis fallax

Z.anienis dahli

Diemenia textilis

Z.amenis gemonensis

Vipera berus

Constrictor constrictor

Natrix viperinus 136

Malpolon monspessulanis 1 60

Thamnophis sir talis

Uromacer oxyrhynchus

Denisonia super ba 110

Bitis gabonica

Natrix natrix

Z.aocys carinatus

Dispholidus typus

laments flagelliformis

Dryophis prasinus

Angle between optic

Width of monocular

Width of binocul

axes, degrees

field, degrees

field, degrees

110

"is

30
34
38

152

24

144

160

26

158

14

158

16

160

18

172

156

18

169

158

18

154

20

144

20
20

172

154

22

160

22

146

32

158

20

20

146

24

28

158

30

158

32

150

32

160

34

168

34

160

38

160

40

40

152

40

40

156

42

42

164

42

46

166

46

VISUAL ANGLES AND FIELDS 295

abundantly under water; and in Cerberus he was unable to detect any
power of accommodation.

Among the birds we may distinguish straight-headed forms like the
pigeon and the song-birds, whose eyes are laterally aimed (Fig. 70, p.
172), from round-headed predaceous species such as swallows, goat-
suckers, hawks, and owls, with more or less frontality — the optic axes
never diverging more than 90° (Fig. 115, p. 309). Some penguins
(Spheniscus spp.) have no binocular field, and consequently weave and
sway a good deal when they are scrutinizing an object. Others, like the
Adelie penguin, look binocularly at far objects and when walking, also
at near objects when they are angry; but they turn the head sidewise and
look monocularly in any calm examination of a near object. Whether
the shoe-bills, toucans, and such birds have had to sacrifice all binoc-
ularity for the sake of their huge bills, is not known.

The parrots have the smallest binocular fields of any so far measured
in birds — 6° to 10° in most species. An exception, of course, is the flight-
less, nocturnal owl parrot or kakapo of New Zealand (Strigops habrop-
tilus) which has strong frontality and a considerable (but unmeasured)
binocular field. Another New Zealand bird is quite unique: the rare
blue or mountain duck, Hymenolaimus malacorhynchus. Whereas all
other ducks fixate monocularly, this species has the eyes aimed forward,
and fixates binocularly like a hawk.

Granivorous birds never have over 25 of binocularity, and many
have less than 10°. The homing pigeon, for instance, has been found
to have a 24 binocular field upon full convergence, with a total field of
340°- 342°. In line with the generalization stated above concerning pre-
dacity, the insectivorous birds and herons have higher values and in the
hawk group the binocular field varies from 35° to 50° or more. Owls
have 60°- 70° ; and considering their marked frontality the hawks and
owls would have even wider binocular angles were it not for the fact that
their monocular fields are so restricted by tubularity. The round-headed
ostriches and their allies also have wide binocular fields but no exact
figures are on record.

The most exceptional birds are the snipes, as exemplified by the wood-
cock. Every hunter knows that in the bizarre 'timber doodle' the eyes are
set far back on the head — so far that the posterior binocular field is prob-
ably much wider than the anterior. The bird's feeding habits afford an
explanation: the long bill is thrust so deeply into the ground after worms
and the like, that the bird would be most vulnerable to attack when feed-

296 ADAPTATIONS TO SPACE AND MOTION

ing, were its eyes not positioned as they are. Another interesting peculi-
arity is seen in the various genera of bitterns. When alarmed, these birds
freeze, with the bill canted up into the air at a steep angle, making them-
selves as tall and slender as possible so as to blend with the rushes among
which they stand. Any binocular field in an anatomically anteriad direc-
tion— that is, along the direction of the bill — would then be aimed use-
lessly at the sky; but the bitterns' eyes can be turned so far ventrally that
they can see binocularly around and under their own chins, and thus
truly forward and parallel to the ground (Fig. 116, p. 309).

The mammals are mostly large enough so that the eyes are carried
well above the ground. Few of them therefore have the optic axes tilted
at all upward as they are in most other terrestrial vertebrates. The excep-
tions are the platypus, some rodents (particularly the beaver), insecti-
vores, bats, a few 'edentates', and the seals. In the platypus, the beaver,
and the seals, the upward tilt is strong and constitutes a definite adap-
tation to keep the eyes in the air while swimming awash. In the whales
there is a marked downward tilt, for these forms have abandoned all
hope of seeing into the air. The sea turtle Chelonia mydas also shows
this ventrad slant of the optic axes, which diverge downward at 150
from each other, in line with the habit of floating at the surface and
keeping watch below for possible food. A similar situation in synento-
gnath fishes has already been mentioned (p. 293).

The angles between the optic axes of various mammalian groups and
species are shown in Figure 113, which brings out graphically the differ-
ences, in this respect, between the pursuers and the pursued. Among the
most defenseless of all mammals are the rabbits, whose optic axes are
nearly in a straight line. The anterior binocular field in different kinds
of rabbits has been found to vary from 10 to 34 . Lindsay Johnson
estimates that a hare has monocular fields of 190°, overlapping both
anteriorly and posteriorly*. The European squirrel, too, is claimed to
see behind him with the eyes at rest. Toward the other extreme there
range the carnivores, with the lords of brute creation, the cats, rivalling
man in their degree of frontality — the axes diverging only from 4° to 9°
in different species. The higher primates seem anomalous in their pos-
session of completely parallel optic axes, for they are not predatory. A

*Indeed, Arthur Thompson states that the brown hare {Lepus europaus) makes a habit
of not looking direaly ahead when running. The animal is credited with keen sight — it is
claimed to watch the eyes of an enemy, and to flee if looked at directly; but it may run
almost into a man, particularly if the latter is standing in a furrow down which the hare
is speeding.

VISUAL ANGLES AND FIELDS

297

totally unrelated and unique habit, that of manipulation, accounts for
the development of frontality by the primates as we shall see later.

The total visual field of mammals varies with the attitude of the optic
axes, from 360 in some rodents through 250 in the dog, to 180° in a
man whose eyes are in the position of rest. The situation in the horse has
been studied with particular care. Here, the temporal boundary of the
visual field runs backward parallel to the axis of the body, so that the
posterior blind area is not angular and constantly widening with increas-
ing distance. Thus the horse — when he holds his head up — cannot be
approached unawares from behind by any object bigger than his own
head. Anteriorly, the limits of the two monocular fields each cross the

Fig. 113 — The angle between the optic axis and the body axis in various mammals. Re-
drawn, modified, from Lindsay Johnson. Families and sample species are shown on the
right side of the chart, larger taxonomic categories on the left.

body axis and make 35.5° angles therewith, thus giving the horse a 71
binocular field together with nearly complete periscopy. Each eye sees
through an angle of 215°, which is probably a record unless it is exceed-
ed in some of the fishes. Some of the special devices which make possible
this wide monocular visual angle in the horse will be mentioned shortly.
According to Kahmann, mammals in general possess binocular fields
ranging in width from 20° (or less) to 40° in the rodents, to 120° or
more in the cats and prosimians and a maximum of 140° in the simians
and man. The ungulates are intermediate with values from 60° to 80°,

298 ADAPTATIONS TO SPACE AND MOTION

as are also the majority of frontolateral-eyed carnivores such as the mus-
telids and viverrids. Among the carnivores, the domestic cat is preem-
inent with (according to ThieuUn) a binocular field of 130° and a total
visual field of 287° — thanks to the large, prominent, and strongly curved
cornea.

Of course, the binocular field of any animal is more narrow above and
below than it is straight ahead, and it is ordinarily pear-shaped. Again,
the cone of binocular space does not necessarily begin immediately at the
eyes — there is often a blind region, in front of the snout (Fig. 128, p.
376), which may extend forward for a fraction of an inch, or for a foot
or more as in Varanus and in large fishes. In chicks, it has been claimed
that it is just this distance (a couple of inches) from which the bird
regards each kernel before pecking at it.

Pisa has studied the domesticated mammals and has mapped the form
of their binocular fields. These tend to be tall, narrow pear-shaped areas
unlike the roundish one of man. In man, the uniocular fields are reduced
to a pair of crescents which are but 30° wide in the horizontal meridian
and taper to points above and below the binocular field. Some of Pisa's
values for the divergence of the optic axes and the maximal width of the
binocular field are given in the accompanying table:

Table X
VISUAL FIELDS IN DOMESTIC MAMMALS (After Pisa, rearranged)

Horse

(Foal).

Cow

Goat

Dogs

Setter

Greyhound. .
Fox Terrier.

Rattler

Guinea-pig

Rabbit

At rest

Aroused

Posterior binocular field.

Divergence of optic
axes, post-mortem

Greatest width of
binocular field

127°

57°

118°10'

62°40'

113°5'

51°40'

103°

63°25'

44° 10'

78°40'

33°20'

82°40'

52°50'

90°20'

40°20'

116°20'

103°25'

76°30'

141 °24'

27°

32°

9°

VISUAL ANGLES AND FIELDS 299

Devices for Enlarging the Binocular Field — Aside from eye move-
ments (which we shall shortly consider) there have been evolved various
devices, both static and dynamic, for enlarging the binocular field despite
the handicap of ocular laterality imposed by the presence of an indis-
pensable snout or beak. These devices are of very diverse nature, but are
best described here under the only heading that unifies them.

Two of them occur in fishes — the aphakic space, and the temporad
movement of the lens in accommodation. The aphakic (i. e., lensless)
space is widespread in teleosts, and often consists of an anterior exten-
sion of the basic circle of the pupil into an egg-shape, with the narrow
end of the egg pointing forward. One can see into the eye through the
narrow end of the egg, past the lens whose center is opposite the big end
of the egg (Fig. 105f, p. 261). It was long debated what the fish saw
outward through the aphakic space; but we now know that he looks
through it only with the temporal part of the retina, and thus through
the lens after all. Were it not for the aphakic space, the line of sight
could not be so nearly parallel to the body axis. Again, when the lens is
drawn backward by the retractor lentis muscle, there is a considerable
temporad component of the motion (Fig. 105). In those fishes which
have a fovea, the fovea is always temporal in location (Fig. 77b, p. 185),
and the lens in accommodation moves temporally more than it moves
backward toward the fundus. This shifts the effective visual axis more
nearly parallel to the axis of the body.

The ungulates are conspicuous for their broad, horizontally oblong
pupils (Fig. 85c, p. 218), which extend the visual field somewhat (see
Fig. 90b, p. 225) in the horizontal meridian (v. re the horse, above) and
hence help to enlarge the binocular field. The frogs, the marmots, and
two carnivores (Cynictis and the Meerkat, Suricata) employ the same
trick, though not nearly so effectively. The snakes Dryophis and Dry-
ophiops, and the probably unrelated Thelotornis, not only have the key-
hole pupil with its aphakic portion lined up with the center of the lens
and the temporal fovea, but also have excavated a groove on the side of
the head in front of the eyes, along which the eye looks ahead (Fig. 79,
p. 186). In Dryophis at least, the lens during accommodation moves not
only forward but also more strongly nasally than in other snakes — a
device which accomplishes, in reverse, the same end as that attained by
the foveate fishes. The transversalis muscle of turtles and lizards (see
p. 279) likewise moves the accommodating lens nasally as well as slightly
ventrally. This is probably of especial help to the lizards, for their eyes

300

ADAPTATIONS TO SPACE AND MOTION

are placed so far laterally, and have so little mobility, that they are in
need of all possible means of converging their visual axes intra-ocularly.
The most conspicuous and common of all of these arrangements is
the static condition which may be termed 'nasad asymmetry', character-
istic of some marine (but not freshwater) fishes, many lizards, all birds,
ungulates and carnivores (e.g. cougar. Fig. 71, p. 173). It expresses itself
in a permanent anatomical tilting of the cornea and lens toward the
snout, so that a line through their centers (the true visual axis) strikes
the retina far temporally from its center. To carry out the asymmetry,
the ciliary body is usually shortened in the nasal quadrant, though some-
times the forward extension of the temporal portion of the retina restores
practical uniformity of width to the ciliary zone in all meridians.

(C) Eye Movements and the Fovea

Kinds of Eye Movements — Except where the eyeball is practically
microscopic (blind fishes, cave salamanders, etc.), the standard set of six
oculorotatory muscles is always present, even in animals whose eyes
might turn but never do, and even in those whose orbits are so snug that
the eyes cannot be turned even passively. Most eyes, of course, can turn
in their orbits; and their movements fall into a classification as follows:

{Always coordinated, so as to appear
conjugated. (In ail vertebrates whose
eyes are mobile at all).

Eye
movements

Spontaneous
(voluntary)

Independent -

With no coordination. (In most
lizards and in birds) .

With coordination in convergence.
(In some fishes and in chameleons).

Conjugate (In mammals exclusively).

Involuntary eye movements, in the sense implied here, are not neces-
sarily either unconscious or incapable of being inhibited, but they are
not willed movements made for the purpose of changing the visual field.
Rather, they are automatic, reflex movements which are intended to keep
the visual field as nearly constant as possible during locomotion and
during passive jogglings of the head and body. In this class fall the vari-
ous 'compensatory' and 'nystagmic' movements. An example par excel-

EYE MOVEMENTS AND THE FOVEA 301

lence is the converse eye movement we make with each movement of the
head when we shake it vigorously in the gesture of 'no'. Whenever this
gesture is made in the course of a face-to-face conversation, we should
find it most disagreeable if the image of the other person, and the whole
visual field, oscillated with our head movements. If the reader will try to
obtain this unpleasant experience by shaking his head without letting the
eyes turn in their orbits, he will find some difficulty. The very act of fix-
ation itself seems to set off any and all eye-muscle reflexes which are
needed to compensate for head and body movements and maintain the
status quo of the visual field.

Actually, the eye-movements of the 'no' gesture, and those made auto-
matically when the head or body is turned actively or passively in any
direction, have their origin in muscles of the neck and in the apparatus
of dynamic equilibrium, in the membranous labyrinth of the internal ear.
Disturbance of this apparatus will disturb the involuntary eye move-
ments, as occurs in vertigo, intoxication, and in artificial situations such
as caloric nystagmus — the induction of convection currents in the laby-
rinthine endolymph by the instillation of hot or cold water into the
external auditory canal.

These involuntary eye movements in man and other vertebrates are
invariably coordinated; that is, the movements of the two eyes are always
in the same sense. If a fish turns sharply to the right, the two eyes rotate
leftward, the right eye turning toward the snout and the left eye away
from the snout. Though the eyes may move independently for the explor-
ation of the visual field, it would never do for them to move unharmon-
iously if the field is to be kept as nearly constant as possible. Where this
is actually impossible of accomplishment, the eyes will still try to hold
on to the field, as in the 'optomotor reaction' so often elicited from lab-
oratory animals for the study of their vision :

The animal is placed on a turntable, in the center of a cylinder coaxial
therewith. The inside of this cylinder or drum bears a pattern, say, of
vertical stripes. If either the cylinder or the turntable is rotated, the
visual field is swept past the animal's eyes. If it is the turntable which
rotates, the animal's labyrinths are naturally being stimulated and we
should expect him to make compensatory movements of the eyes, head,
body, or perhaps all three, in the opposite direction. If only the drum
rotates, there is then no stimulation of the labyrinths; but still the eyes
turn, in the direction the field is moving. This is the optokinetic or
optomotor reaction. When the eyes have swung over as far as they can,

302 ADAPTATIONS TO SPACE AND MOTION

they may periodically jerk to the position of rest and repeat the slow
following-movement. If the animal is one which has little or no eye
mobility, the optomotor reaction will be given by the head itself or, if
this be restrained, by the whole body. This reaction has been much used
in late years (quite improperly!) as a test of visual acuity and as a tool
for the investigation of color vision and still other matters — the assump-
tion being that if the stripes are made so narrow or so much like the
intervening spaces that the reaction fails to occur, the width of the stripes
and spaces look alike to him however different they may look to us, etc.

We perform something essentially like the optomotor reaction, in our
so-called railroad nystagmus. When watching out of the window of a
swift train, we are comfortable enough if we look at distance objects,
which seem hardly to move backward at all as we fly along. But if we
try to watch the roadbed close beside the train we soon experience a
discomfort — our eye muscles are in a turmoil, the eyes constantly jerking
ahead and drifting back in a vain effort to stop the flight of the ties
under the neighboring track.

Voluntary eye movements are those made for exploratory purposes.
In ourselves, they are conjugated, which means something more than
simply coordinated: we are quite incapable of voluntarily moving one
eye independently of the other. The two eyes move together in both
involuntary and voluntary movements, just as though there were a tie-
rod inside the head like that which conjugates the front wheels of an
automobile. There has been exactly one case reported, of a human being
who could move either eye at will. This was a 28-year-old Australian,
described by Sir James Barrett, who could turn either eye outward 20 ,
or both eyes at once — an amazing feat which he had always been able to
do and which "came as natural to him as moving his hand." Our eyes
always move in the same sense, in obedience to certain laws which gov-
ern the interactions of their muscles (Donders' and Listing's laws), for
a change of fixation; but they move in opposite senses — toward or away
from each other — for a change in accommodation. These contradictory
tendencies are controlled from separate centers in the tegmentum, be-
neath the aqueduct of Sylvius (the convergent movements being com-
manded by a special center, the nucleus of Perlia) ; but they are smoothly
blended without conflict whenever we turn our gaze to a new object
which lies both in a new direction and at a new distance.

The system of involuntary and voluntary eye movements is subject to
enormous differences from the human scheme of things, as is hinted in

EYE MOVEMENTS IN FISHES 303

the classification given above. These differences find their explanation
in the presence and absence, and the location, of special retinal regions
of particularly high resolving power. Table III (p. 187) lists these areae
and foveas and should be constantly consulted while reading the ensuing
discussion of eye movements in the various classes of vertebrates.

Fishes — The fishes reveal plainly that the original, primitive function
of the eye muscles was not to aim the eye at objects at all. Their original
actions were all reflex and involuntary, and were designed to give the
eyeball the attributes of a gyroscopically-stabilized ship, for the purpose
of maintaining a constancy of the visual field despite chance buffetings
and twistings of the animal's body by water currents and so on. We will
see later, when we consider the subject of movement-perception, just
how and why this constancy of field is important.

The vast majority of fishes have only the reflex, involuntary, eye move-
ments.* Except in such forms as the rays and flatfishes, these are chiefly
in the horizontal plane. The bottom-hugging rays look mostly up and
down rather than from side to side, and in them the superior and inferior
rectus muscles are better developed than the lateral ones, whereas in their
pelagic relatives the sharks, the lateral recti are the heavier. In fishes
whose eyes sit laterally, every turn of the head is accompanied by a com-
pensatory turning of the eyes. A moving object is never followed by an
eye movement — instead, the fish (having, ordinarily, no neck) bends or
turns the whole body so as to face the interesting object and keep it in
the binocular field. In aquarium specimens, 'wheel' movements of the
eyes can often be clearly observed : as the fish tilts his body in starting
to swim upward or downward, the eyeball makes a compensatory ro-
tation in the plane of its equator. This movement, obviously carried out
by the two oblique muscles, suggests that this was the primitive function
of those muscles.

In a number of species, spontaneous movements are known to occur.
All of these forms which have undergone histological examination (ex-
cept Cory dor as! — see p. 387) have been found to be provided with a
fovea, and there is an excellent correlation between the degree of per-
fection of the construction of the fovea — (in regard to visual-cell con-
centration, exclusion of rods, depth of depression, etc.) and the extent

'••^Retraaive movements of the eyeball, which may perhaps be voluntary, are common enough
in fishes and other vertebrates; but such movements have of course nothing to do with
space-perception.

304 ADAPTATIONS TO SPACE AND MOTION

of the voluntary eye movements. A list of species known to have a fovea,
compiled chiefly from the recent work of Kahmann, follows :

With good fovea :

Girella sp. Julis geofredi

Hippocampus spp. Blennius basiliscus

Siphonostoma typhle Blennius gattorugine

Syngnathus acus Blennius sanguinolentis

Syngnathus tenuirostris Blennius tentacularis

Serranus cabrilla Blennius ocellaris

Serranus hepatus Blennius pavo

Serranus scriba Pholis gunellus

With fovea, or at least the beginnings of one :

Balistes capriscus Trachinus vipera

Balistapus aculeatus Julis vulgaris

Tetrodon fluviatilis Julis pavo

Trachinus draco Agonus cataphractus (?)

These foveate fishes are all marine and inhabit the littoral zone. Some
are characteristically agile and lively in the pursuit of prey, though others
are sluggish, and the pipe-fishes and sea-horses have very deliberate swim-
ming habits. Several of the species inhabit rocky clefts, where their
capacity for eye movements seems a definite advantage in their cramped
quarters. Rather surprisingly, considering its behavior, the archer-fish
{Toxotes jaculator) is not among those which have a fovea; and it will be
recalled (p. 292) that this fish also has a rather narrow binocular field.

In all of the above species except the sea-horses, the fovea is located
strongly temporally, in the retinal region which can see binocularly (Fig.
77b, p. 185). But while these fishes can and do converge their eyes to
aim both foveae at a prey object, the eyes are moved independently and
are not conjugated, but only coordinated temporarily in each act of
convergence. In fact, such fishes are the only vertebrates which can em-
ploy a temporal fovea for monocular vision. In such genera as Blennius,
Serranus, Julis, and Trachinus, either monocular or binocular fixation
may be maintained on an object. The better the fovea, the greater the
tendency to adhere to binocular fixation. The average teleostean fovea
is a shallow pit, far inferior in construction to sauropsidan foveae; but
in Girella, according to Mile. Verrier, it is the equal of the superb fovea
of the chameleons. Some syngnathids have been claimed to have two
foveas in each eye, but Kahmann was unable to confirm this.

Many other species, among those kept in large American aquariums,
can be seen to make spontaneous fixative movements. Most of these have

AMPHIBIAN, REPTILIAN EYE MOVEMENTS 305

a prominent aphakic space (Fig. 105f, p. 261) — so commonly associated
with a temporal fovea — and all of them should be studied histologically.
Examples are: Promicrops itaira, Stenotomus versicolor, Monacanthus cili-
atus, Centropristes striatus, Mycteroperca bonaci, Sphceroides maculatus.
The fishes thus illustrate clearly the universal principle that: where
there is no fovea, or at least a well-defined area of acute vision, there are
no spontaneous eye movements. For, unless one spot of the retina is
clearly superior to the rest in resolving power, there is no advantage
in aiming any one part of the retina at the object of interest, whether the
latter is still or in motion. Only when the object has moved close to the
edge of the visual field will any action be taken to maintain visibility of
it — and then it is by a turning movement of the whole body (or of the
head if a neck is present) , and not by a movement of the eye unless the
optomotor reaction is being evoked. The act of precise fixation, then, is
performed only by areate and foveate animals.

Amphibians — No amphibian is known to perform any eye movements
other than retraction and elevation. ' Since retraction is usually, if not
always, elicited by a contact with the eye or used (by the Anura) as an
aid to swallowing, it is questionable whether it is ever spontaneous. In
turntable experiments, amphibians exhibit the usual compensatory move-
ments and also give an optomotor reaction to a rotating field; but in the
absence of a neck (anurans) these movements are of the whole body.
The eyes do not turn in the orbits at all. Frogs have an area centralis,
but this is a large, vaguely defined, horizontal crescent (in Hyla, a large
circle), whose superiority in resolving power, over the remainder of the
retina, is extremely slight. There is therefore no more need of any fix-
ative aiming of the eye than in the great majority of fishes.

Reptiles — Reptiles may sit for hours without making spontaneous eye
movements; but most species are capable of them, as well as of the full
panoply of labyrinthine and optomotor reflexes involved in the gyro-
scopic maintenance of the visual field.

The crocodilians have not been much studied; but, being nocturnal,
they are probably comparable to the amphibians in the matter of eye
movements. The turtles however, despite the absence of a fovea in all
but Amy da, have a good-enough area centralis to need the power of
fixation. Their lateral eye movements, particularly in carnivorous forms,
are coordinated for binocular observation; but vertical motions are made
independently by the two eyes, which are thus not truly conjugated.

306 ADAPTATIONS TO SPACE AND MOTION

In Sphenodon, and in the lizards except the monitors, the binocular
field is so small, and the fovea so nearly central, that any binocular em-
ployment of the fovea (such as can occur in some fishes) is out of the
question. Lizards on the whole rely entirely upon monocular fixation,
with the two eyes wholly independent in their voluntary movements.
Monocular fixative and exploratory movements are especially conspic-
uous in alert and active lizards such as the agamids, iguanids, and
Z.onurus. But independent spontaneous movements of the eyes reach
their zenith in the chameleons (which are so frequently stated to be the
only vertebrates whose eyes move independently). The extraordinary
mobility of the chameleon eye is the resultant of several factors : the lid
crater around the small cornea restricts the external visual field of the
eye; the visual axis is long and the retinal image relatively large; and the
retina, away from the fovea, falls off rapidly in quality of construction
for high resolving power. The insectivorous feeding habit, in so slow-
moving an animal, requires perfect judgment of distance, necessitating
that the eyes be capable of enough convergence to give the foveae a
common point of aim. The chameleon's eye bulges quite a bit from the
head, enabling the animal to sweep the visual line through a wide angle,
turret-fashion; and it can employ the eyes independently for its perpetual
exploration of the surroundings or, at will, associate them for foveal bin-
ocularity when a prey insect is spotted. The eye can be turned through
180° horizontally, 90° vertically, and one eye may be made to aim back-
ward while the other looks straight forward. By way of comparison,
Lacerta viridis (a typical lizard) has but 40 of eye movement.

We have seen that only the teleosts can use a temporal fovea mon-
ocular ly. The chameleon is also exceptional, in that it can use a central
fovea binocularly. The movements of its body are slow in the extreme —
reminding one of the sea-horses (which also have central foveae and
prehensile tails, and better deserve to be called the 'chameleons of the
sea' than other fishes which have been given that appellation) — but the
sticky tongue is shot out with lightning speed at any insect that settles
within range. As Rochon-Duvigneaud has so well put it : "S'il y a encore
des cameleons, c'est que leur oeil est infaillible."

Many of the more sluggish, less eye-minded lizards, such as the Gila
monster, have fixed eyes; and in the snakes there is but little spontaneous
mobility. It is because of this that the static binocular field of snakes is
wider than that of the lizards whose eyes can move and converge. What
movements the snake's eyes do make are either independent or, in con-

EYE MOVEMENTS IN BIRDS 307

vergence, simultaneous. Like the turtles, the snakes prefer to scrutinize
objects binocularly, and even those whose binocular fields are narrow
will move the head from side to side in pendulum fashion, as if they
were trying the impossible of seeing all of the object with both eyes at
once. Dryophis and Thelotornis, probably Dryophiops as well, have
temporal foveae and enjoy foveal binocularity without benefit of con-
vergent eye movements (see pp. 185-6, 299).

Birds, and the Visual Trident — For reasons which were pointed out
in Chapter 8, the bird eye is even larger than that of a lizard. It is a very
tight fit for its orbit, which could be called roomy only in the penguins
and cormorants. Only these birds, some other divers such as the pelicans
and gulls (and, strangely enough, the hornbills and ground hornbills)
have much eye mobility. Most birds have little or no spontaneous mobil-
ity, relying upon the flexibility of the neck; and even the reflex eye move-
ments may be greatly restricted and replaced by reflex neck movements.
In some cases, the eyes can turn reflexly in the vertical plane but not
when the head is rotated in the horizontal plane. Moving objects are
generally followed by movements of the whole head. Fixation may be
monocular with the central fovea, or binocular for optimal judgment of
distance — even in parrots, whose binocular field is very narrow. Such
spontaneous mobility as there may be is mostly horizontal, and for the
enlargement of the binocular field. Even the hen is capable of this slight
convergence, despite a 144° divergence of the optic axes.

The imperative need for accurate distance-judgement, coupled with
the impossibility of any chameleon-like binocular use of the central
foveae, has led to specializations of the temporal part of the retina.
Some of these are slight, like the 'red field' of the hen; but in many
different groups of birds, independently of each other, a second fovea
has been differentiated in the temporal quadrant. It is present in the
very birds which, one might say from their feeding habits, need it most :
the various hawks and eagles, the humming-birds (Fig. 80b, p. 188),
the swallows, many bitterns, and various passerine wing-feeders. Despite
their close kinship with the hawks, the vultures apparently lack the
temporal fovea. Since they are ground feeders, this is readily compre-
hensible. The extra fovea of the kingfisher is believed to have a very
special significance (see p. 442).

The accipitrine birds, the swallows, etc., thus have what Rochon-
Duvigneaud has called the Visual trident'. They look antero-laterally

308

ADAPTATIONS TO SPACE AND MOTION

with the two central foveae, and binocularly straight ahead with the two
temporal foveae (Figs. 114, 115). A substantial part of the whole visual
field of the bird is thus subtended by highly superior receptor areas. The
sacrifice of lateral and posterior visual field entailed by the frontality of
the eyes is easily made by the hawk (which fears no enemy whether he
can see it approach or not) and by the swallow, which expects to outfly
any challenger.

Except in the eagles and in Apus apus, the temporal foveae are inferior
in construction to the central ones. This seems to hint that in birds
(unlike ourselves) binocular resolving power is higher than monocular

Fig. 1 14 — Dissected head of a hawk, with eye bisected equatorially. After Rochon-Duvigneaud.
cf- central (nasal) fovea; tf- temporal fovea; p- pecten.

— being teamed with its mate in the other eye, the temporal fovea per-
haps does not need the structure of the central one which works alone.
A hawk prefers to turn the head to follow objects binocularly, and can
rotate the head on the neck through a full half-circle. But if the head is
held, the hawk will 'follow' monocularly within the narrow limits of its
ability to swing the eye in the orbit.

The owls have only the temporal fovea. It is an academic question
whether this was once a second fovea and the original, central one has
disappeared, or whether a one-and-only £ovea migrated temporally as the
eyes became more and more frontally aimed, during the evolution of the

THE 'VISUAL TRIDENT'

309

owls from swift-like forms through the goatsucker and frogmouth types.
The situation in Apus (p. 188) suggests that the ancestors of the owls
may have had both foveae. A central fovea would be of little value to a
modem owl; for, owing to the great restriction of the visual angle in the
tubular eye, the angle between its line of sight and that of the temporal
fovea would be a narrow one. The owl eye cannot be turned in the orbit,
even with a pair of pliers. It has been pointed out that these, the most
frontal of all bird eyes, are the least mobile while the most frontal of all
mammalian eyes (our own) are the most mobile. This makes sense how-

Fig. 115 — Projections of the visual fields of a hawk, showing the visual
trident of bifoveate birds. Relative resolving powers are suggested by the
closeness of the hatching, b- binocular field; m, m- residual monocular
(uniocular) fields; x, x- blind region; c, c- projections of the central
fovea; /- common projeaion of the tempxjral foveae.

Fig. 116 — A
bittern, Ixobry-
chus minutus,
in 'freezing'
posture, show-
ing ability to
see binocularly
beneath the
head. Redrawn
from a photo
in LIFE.

ever when it is kept in mind that the owl's head can swivel through 270
or more; and this situation actually does have its parallel among the pri-
mates— in Tarsius, whose tubular eyes are immobile and whose head can
rotate on the neck through an angle of 180°.

The owl is safe enough in the matter of distance-estimation, without
having a visual trident — for it does have the all-important central tine of
the trident; and its almost bat-like ability to dodge obstacles, through the
use of auditory cues, enables it to avoid crashes as easily as does a hawk.
But the necessity of the temporal foveae (with or without the rest of the

310 ADAPTATIONS TO SPACE AND MOTION

trident) for perfect judgment of the distances of objects has been
brought out experimentally in the interesting experiments of Portier on
the Northern gannet, Moms bassana. This bird has only central foveae
and is one of the many fish-eaters which dive after their prey. Such birds,
plunging into yielding water with the beak open or with talons spread,
have only to continue in the right direction to seize their fish — they need
not have good judgment of distance. A falcon, however, stooping for a
rabbit, must know where and when to check its flight or else collide dis-
astrously with the ground. To study the gannet's ability to do this,
Portier fastened fish on top of floating bits of board and then rowed
away to let the birds get a good look. He found that the gannets, diving
upon the fish bait, could not tell where to stop and would even transfix
the soft wood with their beaks, thus trapping themselves. This bird —
often called 'booby' — may not be able to learn much; but the falcon is
not given a chance to learn that the hard earth will kill him. He must
have the equipment for distance-estimation ready-made, and use it
instinctively. The gannet, not being similarly equipped with the complete
foveal trident, could never have mastered the problem Portier set for
him, even if he were far more intelligent than he is.

Clearly, the central foveae are of no value in binocular distance-judg-
ment, but are of use to the flying bird only for seeing and avoiding obsta-
cles while the temporal foveae are kept aimed straight ahead. Birds in
flight are commonly observed to tilt the head on one side to look down
to the ground monocular ly; and this is as true of those provided with the
visual trident as of those which have only central foveae.

Mammals — In the matter of eye movements, the mammals are at once
set off from all other vertebrates by the fact that whenever voluntary
movements are possible at all, the two eyes are never independent but
are always conjugated.

This universal conjugation is associated with the fact that mammals
(whales, rabbits, and some others excepted) examine things only binocu-
larly — even the bats, small rodents, insectivores, and other nose- or ear-
minded nocturnal forms whose eyes never move even reflexly. Where the
eyes are placed laterally as in the rabbits, there is usually no area cen-
tralis, let alone a fovea, and there are no spontaneous movements at all.
But even the rabbits have the gyroscopic reflex eye movements, including
the optomotor reaction. These compensatory movements in mammals are
always most extensive in the plane of greatest biological usefulness, which

EYE MOVEMENTS IN MAMMALS 311

usually means horizontal. The hippopotamus, lying with the eyes just out
of water, is claimed by one author to be able to make even voluntary,
monocular, vertical movements like a sauropsidan. The modern hippo-
potamus has no aerial enemies, or indeed any known enemies at all; so
the value of this 'ability,' if it exists, is doubtful. It may be a necessity,
rather than an ability — imposed by the slender horizontal pupil.

Where the angle of eye movement is small, the lid opening is also
small. One can thus judge the extent of ocular mobility in a given mam-
mal by noting how much of the white of the eye (the sclera) shows.
Spontaneous eye mobility is greatest in the higher primates, which alone
among mammals have a fovea; but even here it is supplemented to a sur-
prising degree by head movements, as we soon find out when we spend a
day with a stiff neck. It is next-best developed in the larger carnivores,
particularly the cat and dog families; but it is not so conspicuous in the
ungulates. It is probably only accidental that voluntary eye movement
seems best developed in the 'most intelligent' mammals, as has been
pointed out by some authors. The elephant, with high intelligence and
little eye movement, seems to be the exception which destroys the rule.

The voluntary eye movements of mammals are really best correlated
with visual acuity, which, it so happens, does go pretty well with intelli-
gence in this group of vertebrates. The mammals obey the rule that such
movements occur only where there is a fovea or a circumscribed and dis-
tinct area centralis. Binocular employment of the two areas (in primates,
the two foveas) is so valuable and so constant that it has become fixed
in the neuromuscular apparatus as an unlearned habit, the expression of
which is the continuous conjugation of the two eyes — so different from
the mere temporary coordination of a fish or a chameleon. Again, the
urge toward binocular vision has operated in evolution to increase the
degree of frontality in the most eye-minded of mammals — the primates
and the larger carnivores and ungulates. In the individual mammal, even,
the urge to see binocularly is extremely powerful. Even in animals for
which it is a great labor, the head is turned to face squarely an object
which has taken the attention. Thus the horse, for example, fixates
objects binocularly until they approach within three or four feet, when
he is forced to turn his head away and continue his observations monoc-
ularly. In cats and dogs, if the insertions of the superior rectus and
external rectus muscles are surgically interchanged, or even if the ex-
ternal is removed and the superior brought down into its place, the eye
movements become completely re-conjugated in a few days. Recent work

312 ADAPTATIONS TO SPACE AND MOTION

on monkeys has shown that all four recti can be shifted about, the eyes
becoming re-conjugated in a few days.* The recovery takes place, though
more slowly, even when the animal is kept in darkness.

It is the predator which visually pursues its prey, and the inquisitive
primate picking up this object and that for manipulation at close range,
which have the greatest need for the accurate estimation of distance
which sharp binocular vision alone confers. Such vision is obviously aided
as much by frontality as by the improvement of the area and the final
creation of a fovea. According to Lindsay Johnson and Elliott Smith, no
non-simian mammal can converge its eyes, though it is perhaps significant
that cats and dogs can be taught to do so — the cat being perhaps closer to
the verge of producing a fovea than other arhythmic mammals. Nicolas,
however, states that the dog converges naturally. Other authors have
claimed that many mammals do converge when excited in the pursuit of
prey or in fleeing from an enemy, thus widening the binocular field when
it will do the most good. Such convergence is not necessarily voluntary,
however. Even in the rabbit, which has no voluntary eye movements, the
angle between the optic axes is less when the animal is excited than when
it is undisturbed (see Table X, p. 298) .

The squirrels, and especially the marmots with their 'universal macu-
larity', constitute a rather special and interesting case. The marmot or
prairie-dog's eyes are strongly lateral and are but slightly movable. But
the retina has everywhere as high a resolving power as many another
animal's fovea, so there is no need of fixative, aiming movements of the
eyes. As Rochon-Duvigneaud has pointed out, the marmot can explore
space without betraying itself by the slightest movement, even of its eyes.
It is thus far from being in the same class with such forms as the rat or
the frog. The latter keep their eyes still not because their retinal reso-
lution is everywhere so excellent, but because it is everywhere so poor.

The case of the marmot is the only one which prevents us from gener-
alizing that the spontaneous eye motility of vertebrates is correlated with
high visual acuity as such. We still must say that such movements occur
only where there is high acuity of vision within a restricted area of the
retina (p. 305), which must be directed toward an object if the latter is
to be seen at all well.

*The investigators (Leinfelder and Black) found however that if the superior oblique was
disturbed there was no re-coordination even after months. The meaning of this is not yet clear.

CLUES TO DEPTH AND DISTANCE 313

(D) Depth- and Solidity-Perception

In the first section of this chapter we considered the methods by which
vertebrate eyes adjust themselves for the distance of the object being
viewed. It was pointed out that this adjustment, accommodation, has
nothing to do with giving the animal an awareness and estimate of the
distance. This awareness of the 'third dimension', or toward-and-away
distances and movements, is a perceptual matter and not, like accommo-
dation, an optical one. Moreover, it is unrelated to the perception of
movements in the other two dimensions of space — horizontal and vertical
displacements of visual objects. This latter kind of perception, which is
movement-perception in the usual sense of the term, is considered in the
next section. Here, we are concerned with the means by which man and
animals judge visually the distances, depth, and thickness of objects; and
with the question of whether, and how, vertebrates perceive solidity —
whether, for any of them, stereopsis is possible as it is for man.

Clues to Depth and Distance — The estimation of distance is an
exclusive monopoly of the sense of sight in all vertebrates except the bats.
It is quite impossible to be sure of distances when walking in the dark,
and our judgment of the distance from which a sound has come is faulty
in the extreme. In human vision, a number of clues exist which we inte-
grate perceptually to arrive at an evaluation of distance and the relative
distances of several objects. Most of these clues are as readily employed
in monocular vision as in binocular — in fact, they are incorporated by
any good artist into his two-dimensional painting in order to promote the
illusion of depth (see also p. 194). But when the two eyes are in use in a
three-dimensional visual field, a special and important factor is intro-
duced which is of particular value when the object is close at hand; and,
of course, it is the closest objects which are most important visually, as
any blind man knows. There is no more vexed question in all of compar-
ative ophthalmology than the one whether this binocular factor in depth-
perception exists for vertebrates below the mammals. But certainly the
same monocular clues that we humans employ are available to all verte-
brates. Whether a given animal can use a particular one of them, how-
ever, depends upon his powers of observation, his learning capacity, and
his equipment of instincts. These monocular clues are :

A. Retinal image size. Where the object is a familiar one, its apparent
size, as determined by the size of its image on the retina, is a cue to its

314 ADAPTATIONS TO SPACE AND MOTION

distance. As an object approaches, it appears to grow. A closely related
cue is:

B. Perspective. All horizontal lines, if produced, appear to meet at the
horizon. An object appears farther away if its horizontal contours are
close to meeting. We know which end of an object is nearer to us, from
the direction in which the object appears to taper.

C. Overlap and Shadow. If one object hides part of a second object,
it must be the nearer of the two. So also if it casts a shadow on the sec-
ond object. The more overlaps there are in a visual field, the greater
seems to be the distance to the farthest object. This is why distances over
water, with no intervening objects, tend to be underestimated.

D. Vertical Nearness to the Horizon. When we are looking at nearby
objects, our line of sight tilts toward the ground. More distant objects
are seen at apparently higher levels, for in looking at them the line of
sight must be elevated.

E. Aerial Perspective. Objects appear farther away if their outlines are
hazy and their surfaces dim or bluish, for long atmospheric pathways
create such appearances. Colors are affected by aerial perspective and
become unsaturated at a distance. Distances through exceptionally clear
air tend to be underestimated; distances through mist, overestimated.

F. Parallax. This, the most important of all monocular factors, is the
change in the apparent angle, at the eye, between a near and a far object,
produced by a lateral movement of the observer's body or head. As we
move our heads from side to side, near objects seem to move extensively
in the opposite direction as compared with far objects, while the latter
seem to move slightly, in the same sense as the head movements, in rela-
tion to the nearer objects. It is chiefly this cue which enables a one-eyed
man to move about in an unfamiliar roomful of furniture without bump-
ing into things any more often than a two-eyed person.

The one-eyed person, however, may have considerable difficulty with
the common parlor trick in which one attempts to bring two pencil-points
together with the arms outstretched. Binocular perception of distance —
shcJrt distance, at any rate — is infinitely finer than monocular. What is
its special basis?

In binocular vision, whenever the eyes accommodate for a particular
distance, they also converge to a degree that aims the two foveal lines of
sight at a common point at that distance. In looking from one object to
another which is at a different distance, the extent of convergence either

STEREOPSIS IN MAN 315

increases or decreases. The amount of convergence, evaluated quite un-
consciously via kinesthetic reception from the internal rectus muscles, is
a potent cue to distance. It is effective up to the greatest distances for
which we converge at all appreciably — up to a hundred feet or more,
which is far beyond the distances for which we accommodate.

The stimulus to converge seems to be the psychic impression of near-
ness. Convergence is then guided to the point of precision by the urge to
unify the two one-eyed images of the object being attended to, with
accommodation tagging along as a dependent reflex. When the object is
seen singly, convergence and accommodation freeze; and the parallactic
angles of convergence of the two eyes, being simultaneously recorded in
the nervous system, afford a precision of distance-judgment which succes-
sive monocular parallaxes can never yield. The perception of singleness
is inseparable from the perception of the distance of the object; and in
fact both are attributed to the object — the latter's distance from us seem-
ing as much a part of the object as its size and shape. In man, at least,
singleness of a solid object is also inseparable from the perception of its
solidity — the psychic process which we call stereopsis.

Stereopsis in Man — Stereopsis means, literally, 'seeing solid'. As a
word, it has been loosely used as a synonym for distance- or depth-per-
ception (which is better known as bathopsis) ; but we can perceive depth
without solidity, or solidity without depth. For the estimation of dis-
tances in the visual field, convergence must be allowed; and it must be
allowed to 'play' or vary back and forth until it finds its dead center on
the object. But the perception of solidity is literally lightning fast, for it
is obtained in a stereoscope even when the pictures are illuminated by a
single electric spark lasting a ten-thousandth of a second. This, 'Dove's
experiment', is conclusive evidence that solidity does not depend upon a
play of convergence, for no time is allowed for that process. Nor is
convergence as such even necessary, for prisms can take its place as they
do in the ordinary stereoscope. As Javal pointed out years ago, the idea
of relief is one thing, and its measurement is another. Estimation of dis-
tance, depth, and thickness is closely associated with the recognition of
solidness, for both involve the idea of tridimensionality; but the one pro-
cess is dynamic and the other, static.

For stereopsis, the prime essential is a particular blend of likeness and
difference between the images on the two retinae, and a particular position
of each image, this position being governed in ordinary experience by the
degree of convergence. But it does not really matter what the positions

316

ADAPTATIONS TO SPACE AND MOTION

of the eyes happen to be, if only the retinal images are of the right kind
and in the right places, even if put there by an arrangement of prisms or
mirrors in an experimental situation.

The two retinal images must either be left- and right-eyed views of an
actual object or, in the case of drawings which are to be observed in a
stereoscope (Fig. 117) they must represent such views of some possible
solid object — even if it be an imaginary geometrical figure or a gimmick
the like of which the observer has never seen. The two single-eyed views
of a solid object can never be identical even if the object is a smooth ball
— unless it is so lighted that it has no shadow which can be seen more

PieTUWE

-P^-W-I

, 1/ s

<a

M

Fig. 117 — Optics of the Brewster-
Holmes stereoscope.

A card, c, bearing a left-eyed image //'
and a right-eyed image ri of some three-
dimensional scene, is observed through
the half-lenses hi, whose prism action so
bends the light rays that the retinal
images are projected to a common place
in space for which the eyes are con-
verged and accommodated. At this place,
a binocular stereoscopic image si is seen.
The screen s prevents each eye from
seeing the picture not intended for it.

fully by one eye than by the other. Yet any two pictures placed in a
stereoscope must be as nearly identical as right- and left-eyed views are,
or they cannot be 'fused' and will be seen doubly or even alternately by
the baffled brain, in the phenomenon mis-called retinal rivalry.

The left eye sees a Httle way around one side of an object, the right
eye a little way around the other. Naturally enough, if these two images
are fused at all into a single central or cerebral image, the rotundity of
the object is perceived. Of course if the object is two-dimensional, it will
be perceived as such; but even so it will be seen singly, through the
fusion of two one-eyed images. Here, no third dimension is created, not
because the object hasn't one but because the two retinal images in this

STEREOPSIS IN MAN 317

case are absolutely identical.* An approach to this situation is obtained
when we look at objects farther and farther away. We can judge their
distances binocularly, with convergence as the chief clue, up to about
one hundred feet; but even far short of that distance all solidity —
where it really depends upon disparate retinal images and not upon our
familiarity with the object — is lost. Such distant objects appear flat
simply because, with the lines of sight making so slight an angle with
each other, the two images we have of the object are not different enough
to yield any rotundity when fused.

Stereopsis, then, results from the fusion or unification of two views
which differ slightly in a particular way and within certain limits. The
object must be seen singly, and this is where the matter of the location
of the images on the two retinae comes in :

The two images of any object-point must fall upon 'corresponding
points' of the two retinae if they are to be fused. The two foveae are cor-
responding points, and if identical small images are falling upon them,
no matter whether they emanate from a single object or not and no
matter in what direction each eye is pointing, those images will be fused.

When a point at any given distance is fixated by both eyes and is
seen singly, there is at the same instant an infinity of other points in
space which are seen singly along with it. Their images are falling upon
corresponding retinal points other than the foveae; and the external,
spatial points themselves determine a complexly shaped hypothetical
surface hanging out in space, called the horopter. There is a different
horoptral surface for every point of binocular fixation, at every distance
and direction. Obviously, the whole matter of horopters can become
hideously complicated, and it is as well for the reader (and the writer!)
that we shall not need to worry much more about them. Suffice it to say
that when you fixate a point across the room, and raise a finger into the
line of fire, you see the finger doubled, because the right- and left-eyed
images of it are not falling upon points in one retina which 'correspond'
with the stimulated points in the other. They could be made to do so if
the finger were amputated and carried out and glued onto the horopter-
of-the-moment. But by merely looking at the finger the two images are
made to slide together into one, for the change of convergence and
accommodation has created a new horopter on which the finger now lies.

*Unless the object is quite small and quite near — say, a calling-card at the near point —
when the images are of course appreciably 'keystoned': for each eye, the card tapers in
the direction of the other eye.

318 ADAPTATIONS TO SPACE AND MOTION

These doubled images are a sign that the object is not at the distance
of accommodation-and-convergence, and their appearance and disappear-
ance (though we are ordinarily totally unaware of them) is a minor
binocular cue to distance. Another kind of double vision also demon-
strates, and more dramatically, our dependence upon corresponding
points : If one eyeball is pressed and wiggled by a finger placed against
the lower lid, the image on its retina is displaced from the set of points
corresponding to those under the image in the other eye, and the visual
field seems to split and become two fields, one of which slides around
over the other as the finger is wiggled. We can unify the two fields only
by allowing the eye to go back into its natural position, which is one in
which corresponding points are stimulated by the object upon which the
attention is fixed. Even Barrett's Australian patient (v.s.) with his re-
markable ability to dissociate the two eyes at will, had continuous
'diplopia' or double vision while doing so.

Diplopia is simply the seeing of one object in two directions at once.
Each point on each retina has its 'local sign' of direction. To take the
centralmost point for example : when this point receives the image of an
object, the brain sees that object in the direction in which, so to say, the
brain thinks the eye is aimed. Having given the neck muscles and the
extra-ocular muscles certain orders, the brain thinks it knows where the
eye is pointing. But if we move the eyeball passively, with a finger-tip,
the brain is deceived — the object in space has not moved, but it is now
imaged on a different spot on the retina which has a different local sign
of direction. This spot is now actually aimed along the same straight-
forward line in which the fovea was pointing a moment ago. The brain
does not know this, for the muscles have not been told to turn the eye.
So, the brain sees the object in a new direction, different from that in
which it is seeing it with the other, undisturbed eye. This new, second
direction is the one in which the object would have to lie to be imaged
where it is on the retina, if the fovea were still pointing dead ahead.

Now, if both cerebral hemispheres, looking through both eyes, are to
see a single object at the same place in space — fuse it, in other words — ■
the object must be imaged upon corresponding points in the two retinae.
This is only another way of saying that the two retinal areas receiving
images of the object must have the same local sign of direction. Whence
arise these all-important corresponding points of the retinas — which,
except for the foveae themselves, are no fixed anatomical points at all,
but pair up in ever-shifting combinations as the fixation is aimed here

THE OPTIC CHIASM A 319

and there in space? The traditional explanation of them is based upon
a certain peculiarity of the mammalian optic nerves :

The Optic Chiasma in Man and Other Vertebrates — In the verte-
brates the optic nerves from the two eyes never enter directly the respec-
tive sides of the brain. Instead, they come together beneath the brain
and cross over or through each other in an x-shaped structure called the
optic chiasma (Figs. 21, 70; pp. 47, 172). From this, they continue to the
brain as the 'optic tracts'. In all vertebrates from the lampreys to the birds
inclusive, all of the optic nerve fibers from one eye cross over in the chias-
ma to form the optic tract of the other side, so that each eye is connected
only with the opposite half of the brain. This is called 'total decussation'.
Similar decussations are very numerous among the fiber tracts of the
spinal cord and brain stem, and there is no discernible reason for any of
them — they apparently just happened in embryos during the early evolu-
tion of the vertebrates, and became genetically fixed in the group. A
vague sort of case might be made out for having the primitive verte-
brate's left eye connected with the part of the central nervous system
which controls the muscles of the right side, for these would be most
important in turning the animal to face a light coming from the left.
But, the left eye is connected with the right brain which owing to decus-
sations in the motor tracts, controls the muscles of the left side. If we
stick to our teleological guns, we are then forced to believe that the first
vertebrates were negatively phototropic, which is most improbable.

In the optic chiasma of the mammals, and only in the mammals, an
important modification occurs. In these animals the decussation of the
optic nerves is partial: some of the afferent fibers from each retina fail
to cross over, and hence enter the optic tract on that same side. In man,
the proportion is just about fifty per cent, with half of the macular fibers
as well as half of the extra-macular ones remaining uncrossed (Fig. 21a).
The fibers from the nasal half of each retina are the only ones which
decussate; and although there is no visible evidence of it, there is a
vertical line neatly bisecting each human retina, which is the boundary
between the retinal area connected with the same side of the brain and
that connected with the other side.

In all mammals, the relative number of uncrossed fibers is closely pro-
portional to the degree of frontality. It is about one-eighth to one-sixth
of the whole in the horse, one-fifth in the rat and in the common
opossum, one-fourth in the dog and the Australian bushy-tail opossum
(Trichosurus vulpecula), one-third in the cat, and reaches a maximum of

320

ADAPTATIONS TO SPACE AND MOTION

50% in the higher primates and a low minimum in lateral-eyed forms;
but even the rabbits have some uncrossed fibers. This relationship is the
'law of Newton-Miiller-Gudden', and holds good only for the mammals.
Outside of that class, there is no case of a partial decussation of any
degree whatever.

Supposed Value of Partial Decussation — A few have thought that
partial decussation arose as a device for preserving, in animals with
frontal or partly frontal eyes, the original status in which the left brain
saw everything that was to the right of the animal and the right brain

Fig. 118 — Illustrating Ramon y Cajal's ex-
planation of the decussation of the optic
nerves, a, situation which would obtain if
the nerves did not decussate: the two halves
of the visual field are transposed, b, the
decussation of the nerves makes the sub-
jective visual field a proper panorama.

Fig. 119 — Illustrating Ovio's correction of
Ramon y Cajal's vievi: since the whole
extent of any object in the binocular field is
seen by each eye, and since the separate
mental images are due to be fused inter-
hemispherically anyway, it makes no differ-
ence whether the nerves decussate or not,
a, without decussation, b, with it.

(In Figs. 118-121 J. the left- and right-eyed aspects of the visual field are respec-
tively indicated by the solid and dotted portions of the visual object [arrow]).

kept watch on the left — the situation which obtains in a lamprey, for
example, where there is total decussation and no binocular field at all.
But this naive view presupposes that the ancient invention of total decus-
sation was somehow of vital importance in the first place ; and, still worse,
it rides rough-shod over the fact that Gudden's law is inoperable in lower
groups despite the presence in them of species with even total frontality
(some deep-sea fishes, owls, and — dynamically — chameleons).

The great majority of physiological opticists have instead seen in par-
tial decussation the essential basis of fusion and stereopsis. The argu-
ment is that since there are no median end-stations in the brain, fusion
must occur on each side and can only do so if each half of the brain

PARTIAL DECUSSATION

321

receives information from both eyes. This ignores the fact that what
reaches each side of the brain is a somewhat lateral view of the object
from the temporal half of one retina and a nearly straight-on view of
the object from the nasal half of the other retina. If any combination
of images in one side of the brain is essential for fusion, it would seem
more logical for evolution to have produced a type of partial decussation
in which the nasal halves of both retinae were brought to one cerebral
hemisphere and the temporal halves to the other.

The conviction that: "no partial decussation, no fusion" has led to
some rather ludicrous corollaries whenever the convincees have been

Fig. 120 — Ovio's inter-
pretation of partial de-
cussation. The mental
image is 'larger (there-
fore better resolved ) '
than where decussation
is total (compare Fig.
119b).

Fig. 12] — Completion of Fig 120 (in a)
and Fig. 119b (in b) by the addition of
the psychic act of inter-hemispheric fusion,
showing that with either partial (a) or
total (b) decussation, the resulting fusion-
image is of the same character (except for
Ovio's difference in 'size', which is here
allowed for the sake of argument).

made to face the situation in the non-mammals, with their indisputable
urge to attain binocularity despite their total decussations. It is intoler-
able for us to observe, centrally, two totally different, unfusible visual
patterns with the two eyes independently. Retinal rivalry at once sets
in (see Fig. 122, p. 332) and a severe discomfort — powerful headache,
or worse — rapidly develops. Having this in mind, it was impossible for
the psychologist Wundt to imagine how a lateral-eyed animal, such as a
fish or lizard, could possibly attend simultaneously to its two independent
visual fields. Wundt believed that consciousness must alternate between
them! Yet, we can give ourselves something like the effect of total decus-
sation by simply pressing the upright hand flat against the nose. Each

322 ADAPTATIONS TO SPACE AND MOTION

eye then sees only fields in which the other eye can never see anyway,
and the crescentic uniocular temporal retinal fields involved are totally
decussated. Still, we are perfectly able to observe 'out of the comers' of
our two eyes simultaneously. There is no alternation, no rivalry, no
attempt to fuse and discomfort from its failure.

The great Spanish neurologist Ramon y Cajal believed that in forms
with total decussation there must be panoramic vision, the visual fields of
the two eyes being subjoined to complete the whole picture of space
(Fig. 118). Without total decussation, he argued, the two halves of the
whole field would be transposed in the animal's mind (Fig. 118a) and
vision would become worse than useless for purposes of spatial localiz-
ation and orientation. He thought that where there is partial decussation,
fibers coming from corresponding points in the two retinae ended up at
single points in the visual cortex, in 'isodynamic cells' which accom-
plished the fusion. This theory might seem reasonable enough where the
foveae are concerned; but all other 'corresponding points' are imperma-
nent and it would take an infinity of isodynamic cells to tie together
all possible combinations of them. The whole matter of corresponding
points is a psychological one, and not anatomical in any way, as the
phenomenon of the substitute macula (v.i.) clearly shows.

Ovio has corrected Ramon y Cajal's idea of the panorama, which was
based of course on the mistaken belief that a binocular field is an excep-
tion rather than the rule among vertebrates. Ovio's diagrams (Figs. 119a
and 119b) bring out how little difference it makes to binocular vision
whether there is total decussation or no decussation at all. Ovio believes
that fusion (by superposition, not by continuity) takes place in animals
with total decussation, since psychic fusion is a joining of the images
in the two hemispheres into one phenomenally median image; but he
goes on (Fig. 120) to explain partial decussation as a device for making
the mental image larger, and 'therefore' better resolved. On this point,
his reasoning becomes very hard to follow.

Ovio believes, with others, that solidity results from bringing together
two disparate views of the object in the same center — i.e. one side (either
side) of the brain — but that a 'psychic act' is still necessary to fuse them
into a single solid image. The psychic act of fusion does not in itself
create the relief, however; for even when we have only one eye open,
that eye is evoking activity in both cerebral hemispheres and these two
cerebral actions are being somehow unified, yet there is no resultant
idea of relief.

BINOCULAR SINGLE VISION 323

If a fusion of right- and left-eyed images in itself creates the impres-
sion of solidity, then the question of whether total-decussation animals
have stereopsis or not hangs simply upon the question: do they have
singleness of vision in the binocular field? For if we complete either
Figure 120 or Figure 119b by indicating the psychic act of fusion we
derive Figures 121a and b respectively; and in them it would seem that
the final result is the same — the fusion of the whole right-eyed view
of the object with the whole left-eyed view. Even if we close one eye, we
are still seeing with both halves of the brain. We still effect a jimction of
these bilateral activities. There is no reason why a fish cannot do like-
wise. The fusibility of images in the two sides of the brain into a 'median'
image cannot conceivably depend upon the character of the optic chiasma.

If solidity crops out phenomenally in the case represented in Figure
121a, why not also in the case of total decussation shown in Figure 121b?
If stereopsis depends only upon the fusion of the right kind of images,
and we find reason to believe that animals with total decussation do have
fusion and singleness in their binocular fields, then (since we know their
images are of the right kind — i.e., right- and left-eyed) we must look for
an explanation of partial decussation other than the firmly-rooted tradi-
tional one that without partial decussation there could be no fusion and
hence no stereopsis.

The Case for Singleness in Animals — Let us consider a fish, which
of course has total decussation and which we will suppose to have no
binocular field at all. He sees a mouse on the bank. He can look at the
mouse with one eye, or turn his body and look at it with the other. In
either case he certainly sets but one mouse, and he has no binocular par-
allactic cue to its distance and no impression of its solidity other than
that afforded by monocular cues. But now an owl, who also has total
decussation but who moreover has a wide binocular field and convergent
foveal lines of sight, also looks at the mouse. Is it reasonable to suppose
that the owl sees two mice? If so, must he aim his talons half-way between
the two 'mice' in order to seize the mouse — or if not, which 'mouse'
shall he aim for?

Eye-minded species have certainly done everything they could do to
gain binocular vision, by making evolutionary modifications of their static
facial and ocular anatomy. Quite apart from the enormous aid it affords
to bathopsis in intelligent animals which might be able to get along with
only monocular cues to distance, binocular vision has a great advantage
over monocular in any animal, as we shall see. But whatever the gain

324 ADAPTATIONS TO SPACE AND MOTION

made by having frontal eyes and wide binocularity, is it likely that ani-
mals would seek it if, to get it, they had also to tolerate a perpetual dip-
lopia? It is far more likely that the vertebrates would long since have dis-
carded one eye and come to have a single, frontal, cyclopean visual organ
like that of the ascidian tadpole. That they have not done so is evidence
in itself that they have always seen singly in the binocular field, that the
'physiologically cyclopean eye' which the psychologists like to talk about,
when they are stressing the singleness and straight-aheadness of human
vision, is not a primate (or even mammalian) invention at all.

If each side of our owl's brain projects its image of the mouse into the
same part of space, will the owl not see one mouse there? Is not his dual
projection to the same place, which could be occupied by only one thing,
what we mean by fusion? Well, no, not quite; for there might be only
superposition of the two mental images of the mouse. This woiild not be
fusion — it would be more like the mess one would have if one projected
onto a screen, superimposed on each other, the right- and left-eyed images
from an ordinary stereoscopic viewing-card. Would the vision of a total-
decussation vertebrate have to be like that throughout his binocular field?
If it must, one wonders again why the animals with two eyes have not
thrown one away or at least religiously kept their two monocular fields
from overlapping.

In ourselves, fusion is not through superposition or even a complete
blending of the whole of one image with the whole of the other. Rather,
it is a sort of mosaic process which is dynamic, with constant shiftings of
the conspicuousness of the parts of the images, little suppressions of one
part of one or the other as the gaze wanders over the object. In those of
us who have a strongly 'dominant' eye, the solid image is mostly the dom-
inant-eye image, with the image of the other eye used to paint in the
solidity, so to say. If binocular vision in the lower vertebrates yielded a
singleness whose basis was superposition rather than mosaic unification,
then their perception of the form and pattern of solid objects ought to be
far better with one eye than with two, for the superposition of disparate
images would be tantamount to diplopia. But blennies, and chameleons,
and birds with temporal fovese, and mammals all look at things binoc-
ularly from choice, even though, if they wanted to, they could look
monocularly just as lizards are forced to do by their adherence to a
centrally-positioned fovea. Yet, none of these animals is ever observed
to close one eye in order to get a better look!

BINOCULAR SINGLE VISION 325

On logical grounds alone, we can thus make out a strong case for
believing that the lower vertebrates have singleness of perception of
objects in their binocular fields, despite their independent eye movements,
and their lack of any system of corresponding points, and their total
decussation. The mammals, though ranking higher, seem at first glance
to have lost, not gained, something. They are unique in having in com-
bination just these things that the other vertebrates lack — conjugate eye
movements, dependence for fusibility upon corresponding points, and
partial decussation. We shall see that this combination of mammalian
peculiarities expresses a relationship of cause and effect, and that it does
represent a gain of something after all.

It is not known whether lower vertebrates can make binocular color
mixtures (see pp. 90-1), though if they can do so it would require us to
believe in fusion for them. And, the matter should be susceptible of
experimental attack. A fish might be trained positive to purple and neg-
ative to red and also to blue. Provided then with a red covering over one
eye and a blue one over the other, and placed in white surroundings, he
might or might not give a positive 'purple' response; and if he did do so,
it would indicate fusion. But apart from strictly visual phenomena, there
are many indications that the two eyes are interconnected through the
nervous system even where total decussation of the optic nerves obtains :

In some fishes at least, one eye can control the dermal color changes
of the whole body as well as the two eyes normally do (p. 532). In the
rays, there is a consensual pupil reflex — both pupils contract when only
one eye is illuminated. In the pigeon, recent work has shown that there
is not only a consensual pupil reflex but that usually the two eyes blink
when one cornea is touched; and the two nictitating membranes also act
consensually. Moreover, in all vertebrates the two eyes are coordinated
in their reflex movements, though of course this association of the eyes is
strictly motor and has in it nothing of the photosensory element which
exists in the control of the pupils and of the dermal chromatophores.

All in all, there is considerable reason to believe that the binocular
vision of all vertebrates is single vision. The 'independence' of the eyes
due to total decussation has been much over-rated. There is such an inde-
pendence, on the motor side; but this does not make it inevitable that
there shall be sensory independence as well. After all, our two hands
move independently, but when they both grasp the same object its single-
ness is appreciated without benefit of any partial decussation of the spinal
sensory tracts. In the tactual modality of sensation, there is even an

326 ADAPTATIONS TO SPACE AND MOTION

analogy for corresponding retinal points, for if two adjacent fingers be
crossed out of sight and a pencil rested between their tips, two pencils
will be felt in the well-known 'Aristotle's illusion'. Singleness, in the
realm of touch, is obviously entirely psychological in basis. In vision,
it is equally so — and would never have been thought to be otherwise if
the partial decussation had never been discovered by anatomists.

If the total-decussators do have fusion, then as we have seen above
there is no reason to deny them binocular stereopsis. If there is single-
ness created from right- and left-eyed images, stereopsis comes along
with it as a sort of psychological windfall.

The Evolution of Binocular Vision — The need for something can-
not operate as a cause of it; but we do have a right to ask ourselves just
why binocular vision has ever evolved in the first place. What does it
give the animal? Clearly, its adoption and extension involves a loss of
periscopy and must offer some compensations which outweigh that sacri-
fice. In ourselves, the chief advantage of binocularity appears to be a pre-
cision of object-localization. It does not matter that we see solidly, so
long as we see deeply and can say with assurance that one particular
billiard ball is two and one-half inches farther away than another. We
have this ability only because our two one-eyed images are projected to a
common meeting place in space; but independent convergences of our
two eyes would still give us parallax on an object, enabling us to locate
it more promptly and accurately than we can do with a succession of
monocular parallaxes, even if we did not perceive solidity.

We may be sure that animals have not evolved binocularity in order
to see solidly. As we have seen, the percept of solidity came to them
as an incidental accompaniment of disparate-image-fusion. But they
nevertheless have had a powerful incentive to develop binocularity where-
ever their snouts and their beaks and their requirements of periscopy
would permit. This incentive was the fact that the binocular parallactic
cue to distance makes no demand upon intelligence. It is as automatic
as geometry. On the other hand, for the successful employment of the
monocular cues (pp. 313-4), learning to use them is a prerequisite:

A human child must learn slowly to evaluate the size of his retinal
images. To him, a monster airplane a mile in the air seems like a bird a
few yards overhead. He has to be told why the railroad tracks seem to
come together, must learn the meaning of shadows. He slowly learns to
evaluate aerial perspective, and may be painfully deceived by it when he

EVOLUTION OF BINOCULAR VISION 327

Starts to hike to a mountain which looks two miles away and is nearer
twenty.

But long before it has had time to learn any of these lessons, an infant,
not yet able to speak, can employ binocular parallax to reach accurately
for a toy. A chick reacts correctly to distance as soon as it is hatched.
Considering their greatly inferior mental equipment, were not the lower
animals fortunate to hit upon a cue to distance which required no learn-
ing for its successful employment, but merely a reflex coordination of
the muscles of locomotion with the muscles of the eyes?

Of course, in many animals which give every evidence of depending
upon binocularity, the eyes are so close together that they cannot pos-
sibly have much parallactic 'leverage' — the angle between the lines of
sight, at any great distance, is so small that the binocular cue to distance
seems of low value as compared with our own. And, their two views of
an object at any great distance are so nearly alike that their stereopsis
can only be relatively weak. But — an intelligent lion, looking at our (to
his mind) small heads and ridiculously small interpupillary distance,
might say the same unkind things about the usefulness of our binocular
vision. After all, a small animal may have descended from a larger one,
retaining the same facial conformation. A half-pint galago has the same
frontality as a dreadnought gorilla, but only a fraction of the gorilla's
interpupillary distance. Neither of these species represents the size of the
extinct primate which originated primate frontality. Then too, small
animals feed on small objects; and, their absolute speed being low, only
small distances mean much to them from moment to moment of their
existence. Within these small distances, the angle between the lines of
sight of their close-set eyes may be just as great as the one between our
own visual axes when we look yards ahead at an object in our own path.
And it is this angle, not the linear interpupillary distance,* which really
counts.

We can set up a rather complex series of *ifs', as follows :

(a) If vertebrates have sacrificed the ancient periscopy to evolve bin-
ocularity, it must be because it offers advantages; but

(b) If they have binocular vision of an object, they would gain abso
lutely nothing from binocularity if they saw the object diplopically; so

*The interpupillary distances of some of the larger animals may be of interest here. Years
ago, Berlin published the following figures (among others) : young African elephant, 49 cm.;
horse (average of 20), 19.6 cm.; cow, 18 cm.; axis deer, 14 cm.; llama, 12 cm.; chamois,
10 cm.; goat, 9 cm.; sheep, 8 cm.; man, 6 cm.

328 ADAPTATIONS TO SPACE AND MOTION

(c) If they see the object singly with two separate eyes, they must
have fusion of the two images of the object. Now:

(d) If they have fusion, they have parallactic localization of the object
in space; and

(e) If they have fusion of their disparate right- and left-eyed views of
a solid object, they have a percept of its solidity.

But if all these ifs are true, they still leave unexplained why the optic
nerves became incompletely decussated in the mammals. If our reasoning
so far is correct, partial decussation is no prerequisite at all for fusion
and stereopsis. What, then, does depend upon it, and what special
ability has it given to the mammals which lower forms do not possess?

It has already been pointed out that partial decussation is associated
with conjugate eye movements and with corresponding retinal points or
fixed local signs of direction. If a fish with unconjugated eye movements
can look at an object now with the eyes in one position, now in another,
there are surely no fixed local signs of direction in the retina of the fish,
and no corresponding points. And, if a dog can see a rabbit singly with
one degree of convergence at first, and with another degree when he has
become excited by the chase, there would seem to be no corresponding
points involved. But where the eyes have become completely conjugated
in their movements, so that looking to a certain distance always means
a particular degree of convergence, then fixed local signs of direction,
or correspondency of points, could logically be evolved and could never
be detrimental so long as the conjugation remained perfect.

When conjugated eye movements were evolved by the mammals, this
led to the freezing of local directional signs, which then ceased to depend
upon the position of the eye in the orbit. This in turn made the mammals
dependent upon the system of corresponding points for the maintenance
of fusion. How, then, did the conjugation itself arise? Well, if we wanted
to revise the nervous system of a fish or a bird to facilitate conjugation
of the eye movements, we could not do better than to connect each retina
to each of the nerve centers which in turn are connected with the muscles
of both eyes. Then, community of vision of the two eyes could be most
conveniently made to result in community of action. With the two eyes
seeing the same thing, it is optically desirable that they each face it
squarely. If, when one eye aims at and accommodates for a particular
point in space, the other eye automatically aims at and accommodates
for that same point (even if covered, or even after the eye-muscles have

EVOLUTION OF BINOCULAR VISION 329

been surgically scrambled — ^pp. 311-2) we then have a situation superior
to that in, say, the chameleon, each of whose eyes has to locate the prey
insect by itself before the cerebral navigator can work out the position
of the insect by a process of triangulation.

Partial decussation of the optic nerves accomplishes just this desirable
tying-up of both retinae to both the left-brain and the right-brain centers
of eye-muscle control. In the thalamus, not far from the groups of nuclei
which operate the eye muscles, there are way-stations on the sensory
pathway from the retina to the cerebral cortex. These way-stations, the
lateral geniculate bodies, are connected by way of the superior coUicuU
with the nuclei of the eye-muscle nerves. Here, then, is the real terminus
of the optic nerve fibers so far as concerns any importance of the fact
that they come into each side of the thalamus from both retinae instead
of from only one. The fact that in the higher vertebrates ^/-retinal im-
pulses continue on up to each half of the cerebral cortex then becomes
altogether meaningless; for in whatever patchwork fashion the two op-
tical images finally arrive at the cortex, the two (left and right) cortical
image-patterns are due to be fused into one pattern anyway. The whole
aim and goal of partial decussation has already been attained down in
the thalamus and the tegmentum, where what one eye is seeing is enabled
to control the motor impulses to both sets of eye muscles.

Partial decussation is thus explained, not as the indispensable basis of
binocular single vision, but as a logical eventual consequence of binocu-
larity. Its value is not in the immediate field of conscious sensory phe-
nomena at all, but in the realm of motor activity where it serves to facili-
tate the motor cooperation of the two eyes. Partial decussation has never
arisen in the owls or the frontal-eyed deep-sea fishes, perhaps not because
(or not only because) these are not mammals, but because their eyes are
motionless.

The evolution of their motor conjugation has made the mammals
completely dependent upon it for singleness of binocular vision and for
accurate space-perception, for along with it there arose the phenomenon
of corresponding points. This dependence is at once spot-lighted when
anything goes wrong with an eye muscle or its nerve, and a strabismus
or squint develops — one eye turning out or in so far that diplopia occurs.
We can perhaps best understand the relation of corresponding points to
eye-movement conjugation, and understand how the lower vertebrates
get along without both, if we consider the phenomenon of the substitute
macula.

330 ADAPTATIONS TO SPACE AND MOTION

Invariably in a strabismus patient the fovea of the inturned eye loses
its directional sign; but occasionally a patch of the nasal retinal periph-
ery, which is now aimed into space along a line parallel to the other eye's
visual axis, takes on the quality of a corresponding spot paired with the
fovea of the good eye. The previous diplopia slowly fades away and the
patient becomes capable of fusing the image on the fovea of the normal
eye with that on the 'substitute fovea' of the squinting eye. If now the
squinting eye is straightened by an operation, its fovea will regain its old
community of direction with the fovea of the other eye, and temporarily
there will be a monocular diplopia in the operated eye — until the latter's
substitute macula has had time to 'fade' and regain its original notion of
direction.

These processes, under favorable conditions, may require weeks or
months. We can describe the essentials of what has happened, by saying
that a spot on the retina of the squinting eye has taken on a new local
sign of direction because the eye has taken a new position in the head,
with the result that the same objects, in the same places in space, are now
seen in those same places, as before. When we have said all this, we have
really also described what happens in the lower vertebrates with total
decussation, when they perform their independent eye movements. The
only difference is that the alteration of local directional signs is contin-
uous and instantaneous as the animal turns the eyes about, while in man
the local signs are so firmly fastened to particular retinal points that
changing them is an extremely slow process and is seldom possible at all!
The mammals indeed lost something when they developed the partial
chiasma for the sake of conjugating their eye movements.

In conclusion, then : the vertebrates which have much of a binocular
field have always had singleness of objects in that field, and perceive
them as 'solidly' as their inter-pupillary distances allow. The need of a
permanent coordination of eye movements for rapid and precise estim-
ation of distance was finally met in the mammals by the device of partial
decussation in the optic chiasma, putting the oculomotor apparatus in
control of the pair of images and making it responsible for the main-
tenance of fusion. Conjugation being attained, a system of fixed local
retinal signs of direction could now develop, with a consequent improve-
ment of the precision of localization through the appearance of a new
cue to distance — the physiological diplopia (and haziness) of objects
which are off the horopter, and which only disappears when convergence
and accommodation have hit their mark precisely. But, the animal now

NATURE AND BASIS OF FUSION 331

being utterly dependent upon the stimulation of corresponding points
for his singleness of vision, his perception of space and his visual com-
fort are at the mercy of any slightest pathological or traumatic disturb-
ance of the neuromuscular tie-rod which, at his bidding, turns his team
of eyes.

The Nature and Basis of Fusion — By this time, the reader may have
in his mind a rather confused idea as to what 'fusion' actually is. Where
the separate monocular images are perfectly identical, as when two prints
from the same negative are placed in a stereoscope, the binocular fusion-
image differs in no way from the monocular image on either side. The
fusion-image could be adequately represented by projecting on a screen,
superimposed on each other, the two pictures on such a stereoscope card.
But this is a special case — ordinarily, the objects at which we look
binocularly have depth or thickness, and our two monocular images of
them are not identical. We have noted above that the pattern of the
everyday binocular fusion-image is not such that it could be represented
by mere superposition of the monocular images. We can perhaps imagine
that in some way the whole of a right-eye image is integrated with the
whole of a slightly-differing left-eye image, without this resulting in an
effect like that of superposition. But is the fusion-image, whether tri-
dimensional or flat, of this all-of-right-plus-all-of-left character?

If it really were, then we should expect to find in binocular vision two
phenomena which it does not in fact exhibit : {a) binocular visual acuity
should be greater than monocular*; {b) binocular brightness should be
greater than monocular. Neither of these things is true of human vision
in general, though there does seem to be some summation of the monoc-
ular brightnesses in intensities close to the rod threshold. If binocularity
in itself conferred higher visual acuity, or increased the overall sensitivity
of the visual mechanism to light, then these great advantages would
alone be enough to account for the repeated evolution of binocularity
by both diurnal and nocturnal vertebrates of all sorts. The parallel visual
axes of such forms as the owls, galagos, and deep-sea fishes have indeed
been very often explained on the assumption that the binocular-vision
phenomena of such animals include a summation of the two monocular
brightnesses. And we have seen reason to suspect that binocular acuity

*Binocular visual acuity in this sense, which is the resolving power of the two eyes together
as compared with that of one eye alone, is not to be confused with the more common term
'stereoscopic visual acuity'. This latter term refers to the accuracy of binocular distance- or
depth-perception.

332

ADAPTATIONS TO SPACE AND MOTION

may be 'summated' in some vertebrates even though it is not in our-
selves (see p. 308).

It seems odd that binocular resolving power should not be always
higher than monocular. When we consider that the receptor mosaic of
one retina, like a halftone reproduction, can register only certain of the
points on an object's surface, then obviously the chances are prepon-
derant that at any one moment the other retina will be recording a set
of points which fall mostly in between those of the first set — just as one
retina 'fills in' the blind spot produced by the head of the optic nerve
in the other retina. If now the two sets of object points are interdigitated
in a fusion-image, why is not that image as well resolved as would be the
monocular image supplied by a retina containing nearly twice as many
receptors per unit area as either member of the pair of retinae we are

Fig. 122 — Retinal rivalry for patterns,

a, stereoscope card bearing unlike patterns, b, the sort of mosaic which one may see, at
any one instant, while observing a in a stereoscope.

considering? One would expect this, just as one expects to gain a better
idea of the form and texture of an object by holding it in two hands
instead of in only one. The bothersome fact remains that when the two
eyes are in use our resolution of details is just as good as, and no better
than, the resolution afforded by the better of the two eyes when that
eye alone is used.

This calls for explanation. We can offer a weaselly sort of teleological
reason why binocular brightness should not be raised over monocular —
at least in diurnal animals, such as man: if binocular brightness were
allowed to be higher than monocular, contours would be created between
the binocular and uniocular visual fields, and these might be as per-
petually disturbing as those seen by a person who cannot get used to

NATURE AND BASIS OF FUSION 333

his bifocal spectacles. But there seems no reason for the evolution of a
special central mechanism for inhibiting any enhancement of visual acuity
that might accrue from the integration of the two monocular images.

That integration must, then, be of a sort which somehow makes
impossible any real interdigitation of two complete monocular sets of
image points in a therefore-twice-as-well-resolved binocular image. This
condition will be satisfied if the fusion image somehow partakes of the
nature of a gross mosaic. And that it does do so, at least where fusion of
patterns is concerned, is suggested by the phenomenon of 'retinal rivalry':

Suppose we observe in a stereoscope (Fig. 117, p. 316) a card, the two
pictures on which are like those in Figure 122a. We might reasonably
suppose that the two sets of diagonal lines would be fused into a perfect
grid; but they are not — what we see is a mosaic, composed from the two
sets of lines, which constantly shifts but which, at some one instant, might
look like Figure 122b. At no time do we see a standing grid pattern,
either throughout the whole square or even in some small area thereof.
Instead, the two unlike patterns vie for a place in consciousness, and at
any one time parts of each pattern are wholly successful.

The image in such situations is generally deemed the very apotheosis
of a non-fusion image. But there has long been a theory, favored by a
minority of psychologists, that the everyday binocular image partakes of
the same ever-changing mosaic character as the rivalry image. It only
fails to exhibit rivalry (and hence fails to reveal its mosaic character)
because the two images being dovetailed together are identical or (where
the object is tridimensional) only slightly unlike — never as greatly dif-
ferent as are the two patterns of Figure 122a. Intra- and interhemispheric
fusions are thus essentially the same, for both involve putting left- and
right-eyed fragments side by side in the total image (Fig. 121a, p. 321).

This mosaic theory of fusion has not yet had an adequate experi-
mental test, but it holds considerable promise. However, though it
accounts beautifully for the equality of binocular and monocular acuity
and brightness, it is helpless to explain the binocular mixture of colors.
One can obtain rivalry between, say, red and green monocular areas in a
stereoscope. But under proper conditions the red and green fuse into
homogeneous orange, which is not of heightened brightness, and yet has
no appearance of being a mosaic of red and green. It would seem that
the single images resulting from the binocular fusion of complementaries,
or of other miscible colors, must of necessity represent the fusion of all
of the right-eye image with all of the left-eye one.

334 ADAPTATIONS TO SPACE AND MOTION

The fusion of pattern and the fusion of color thus seem to be two
very different kinds of fusion. But though both pattern vision and color
vision are equally attributes of the retinal cones, there is room for be-
lieving that they reside in different parts of the central nervous system
(see also pp. 521-3). On each side of the brain there may be two distinct
fusion centers, one being for pattern and the other for color. In such
centers, should we find them anatomically, we should have a basis for a
perhaps entirely physiological fusion of impulses stemming from both
retinae. The basis of the psychic act of fusion (see p. 322) of the two
fusion-images (one in each side of the brain) into one cyclopean image —
and the basis of this, the only kind of fusion present in species with
binocular fields but with totally-decussated optic nerves — would be still
to be sought, presumably in an inter-hemispheric interchange of infor-
mation through commissures.

There is, indeed, good neurological evidence for the existence of two
binocular fusion-loci in each half of the mammalian brain. One of these
may be the residence of pattern fusion, the other of color fusion, and we
can even hazard a shrewd guess as to which is which. In the past two
or three decades many neuro-anatomists and neuro-physiologists have
come to agree that the right- and left-eye pathways, which are separate
in each optic tract, maintain their separateness past the synaptic center
in the lateral geniculate nucleus, all the way to the visual cortex in the
area striata of the occipital lobe. Here, 'layer IV' of the general sensory
cortex — the layer in which awareness in general resides — is triply lam-
inated in primates, and locally presents so-called supragennari (IVa),
mesogennari (IVb), and infragennari (IVc) sub-layers (Fig, 123).

Studies of the brains of traumatic and experimental one-eyed indi-
viduals, in man and other species, have shown that the infragennari
lamina receives only fibers which, coming from the lateral geniculate
body of the same side of the brain, are there connected with optic-tract
fibers hailing from the retina on the other side of the head. Total decus-
sation being the primitive situation, the infragennari layer is likewise
primitive, and its physiological counterpart could presumably be iden-
tified in any vertebrate which has a visual cortex at all. But the supra-
gennari layer, or its equivalent in non-primates, receives only fibers con-
nected with uncrossed optic-tract fibers. This layer is lacking in the
cortical areas upon which the uniocular fields are projected, and is of
course greatly reduced in species whose binocular visual fields are narrow.

NATURE AND BASIS OF FUSION

335

Images presented
separately to the
eyes, as in a ster-
eoscope

Infornnation trav-
eling in optic
nerves

Hue synthesized
(though not per-
ceived) here?

Infornnation trav-
eling in optic
radiations

Stereoscopic half-
image resulting
from intra-hemi-
spheric fusion of
patterns

- /wo
miscible colors

Optic chiasma

Sup. colliculus
Optic tract

„ Lateral geniculate

nucleus

Optic radiation

Lnmince of layer
EZof the visual
«- cortex^he striate
area) in the occ-
ipital lobe

Complete stereo-image
resulting from psychic
acts of re -inversion and
inter-hemispheric fusion

Fig. 123 — Afferent visual pathways and events in binocular vision, in primates. (In most
other mammals the laminations of the lateral geniculate and of layer IV are less clear-cut).

336 ADAPTATIONS TO SPACE AND MOTION

The mesogennari layer is unique in the presence there of numerous
'star' cells. It is not disturbed, but both the infra- and supragennari
layers are subject to atrophy, if the receptors connected with them are
removed. Thus for example, in the brain of a man who has lived for
some time minus his left eye, the left supragennari and the right infra-
gennari laminae of layer IV will be found to be atrophied.

The implication of the sandwich-like morphology of layer IV is that
the mesogennari layer is the locus not only of some or all of visual
consciousness, but also of the fusion of ipsilateral and contralateral
information sent by the two retinae to the top and bottom layers of the
sandwich. The mesogennari layers of the two sides of the brain thus
constitute, taken together, the 'binocular center' which earlier (pp. 90-1)
we saw to be always employed even when one eye is used alone. Again,
both mesogennari layers are involved even in 'hemianopic' vision. Each
of them represents one half of the whole visual field (consult Fig. 123).
Now, if the right or the left optic tract is severed by injury or disease,
the individual is thereafter blind in respectively the left or the right half
of his erstwhile visual field. Even so, he can experience contrast effects
between his seeing and his blind fields. Thus, if he looks at a bright
surface long enough to develop an after-image, he will have a bright
after-image in the blind half. Similarly, if he looks at a colored surface
he 'sees' the complementary color in his blind field, and in turn the
complementaries of both of these colors in the two halves of a chromatic
after-image. Only an interaction of the two sides of the cortex could
account for such phenomena.

A fusion of left- and right-eyed information thus occurs in each
mesogennari layer, and between the two mesogennari layers an inter-
hemispheric fusion takes place, creating the cyclopean image — whether
this be flat or stereoscopic. Presumably, if a symmetrical lesion should
destroy either both infragennari layers, or both supragennari laminae, the
individual would retain a complete visual field (so long as both eyes
were open), but would no longer see stereoptically. No clear-cut case
of this sort has yet appeared in the neuropathological literature.

In man, layer IV appears to be the locus of the entirety of visual
awareness. At least, if the areas striata, or the whole occipital lobes,
are destroyed, the result is total blindness. Something of vision might
remain, of course, if only layer IV were selectively destroyed — we do
not know, since this never happens accidentally and would be impossible
to accomplish experimentally. In lower animals, certainly, some aspects

NATURE AND BASIS OF FUSION 337

of vision persist even after the loss of the whole of both occipital lobes.
Rats, and even monkeys, can make discriminations of differences in
intensity after bilateral occipital lobectomy. Removal of one lobe should
theoretically produce no change except to create hemianopia — vision in
only half of the field — but it has been claimed that in the chimpanzee
there is a slight but permanent impairment of visual acuity following
unilateral occipital lobectomy. In man, mild lesions of one or both areae
striatae alter or destroy color vision in half or all of the visual field, but
achromatic sensations remain intact unless the lesion is more serious —
the sense of brightness being particularly durable. Here again, we have
evidence that hue is recorded centrally by a mechanism distinct from
that mediating the remainder of vision.

As regards intra-hemispheric binocular fusion, it might seem that both
color-fusion and pattern-fusion would have to occur in the mesogennari
lamina. Consciousness of the products of the fusion-processes assuredly
occurs only there, in man. But it is quite possible that some visual
information from the two eyes is mixed together below the brain-level
at which it gets into consciousness. In the highest vertebrates, the lateral
geniculate nucleus affords a one and only opportunity for such pre-
conscious mixture:

The lateral geniculate (Fig. 123) is the only way-station on the path-
way of visual sensory impulses from retina to cortex. In the optic nerves,
the fibers are in fascicles, each representing a spot of retina; but in
going through the chiasma these bundles fray out. By the time the
crossed and uncrossed fibers enter the lateral geniculate body, they are
so intermingled that just about every crossed fiber has an uncrossed one
running alongside it. Within the lateral geniculate, the synapses with
geniculocortical fibers are intimately intermingled in an elaborate lamin-
ation which gives the geniculate a rather more complex structure than
even the cortex itself. This multiple lamination of crossed and uncrossed
synapses implies that some aspect or aspects of binocularity are handled
in the geniculate, as otherwise the interweaving, there, of the right- and
left-eyed optic pathways seems meaningless in view of the fact that they
must later be untangled again in order to enter the laminae of layer IV
independently.

It appears, then, that the synthesis of monocularly or binocularly
mixed colors may very well be accomplished in the geniculate, so that
although there is no awareness of the color until the cortex is attained,
the information carried through the optic radiations already has the

338 ADAPTATIONS TO SPACE AND MOTION

colors mixed. The (mosaic?) fusion of brightness-patterns in the meso-
gennari layers follows, and the total picture of visual space is synthesized
through the inter-mesogennari connections in the corpus callosum.

Speaking against this view is the fact that color vision is so much
more readily disturbed than brightness vision, by cortical lesions. The
anatomical facts will fit, as well, an alternative hypothesis that it is
pattern which is fused in the geniculate, color in the mesogennari layer.
In rats and monkeys, consciousness of the brightness patterns, whether
already fused there or not, resides in the lateral geniculate. And, the cat,
which has no color vision, has almost as complex a geniculate as man —
and therefore, in the cat (and hence in man?) its structure cannot be
purposed to accomplish color mixture.* In any case, upon the culmi-
nation, in man, of a completely equal representation of the two eyes in
each side of the brain, consciousness seems to have been made to wait
upon intra-hemispheric fusion, and both processes have been pushed up
into the cortex insofar as achromatic sensations are concerned. In
animals which have totally decussated optic nerves, and hence have no
intra-hemispheric fusion to be accomplished, the whole of visual con-
sciousness is enabled to sit at a relatively low level (ordinarily the optic
tectum — see p. 522) of the central nervous system.

The Strange Fate of the Median Eyes — One of the conclusions
reached above (that the vertebrates have always had single vision in the
binocular fields of their lateral eyes, whatever the structure of the optic
chiasma) may shed some light on the curious history of the median eyes :

There are indications, from elasmobranch embryology, that the pro-
vertebrates possessed a metameric series of paired visual organs on the
roof of the head. Most of them rapidly disappeared as the lateral,
ordinary eyes became perfected; but two pairs of dorsal eyes still hung
on almost until the cyclostome level of evolution was reached.

In most modern cyclostomes, two dorsal eyes are present (Fig. 124).
They do not represent a pair, however, for they are arranged in tandem
with one behind and below the other. Neither is squarely on the mid-line
of the head — instead, one appears to join the roof of the diencephalon
to one side, the other on the other side, of the sagittal plane. These two

*Le Gros Clark has recently suggested that the six layers of the primate lateral geniculate
(three conneaed with one retina, three with the other) are related to the three fundamental
hue-sensations described by the Young-Helmholtz theory (see pp. 91-6). This is hardly
possible, since cats, phalangers, and other nocturnal, achromatic mammals also have lam-
inated geniculates — sometimes even with odd numbers of layers.

HISTORY OF THE MEDIAN EYES

339

sub-median eyes of the lamprey, the 'pineal' and 'parietal', thus seem
each to represent one member of an original pair (Fig. 54, p. 126). In
the same way, the one eye of the ascidian tadpole (see p. 121) is situated
off the mid-line and seems to have a mate in the form of a vestigial mass
of tissue on the other side of the head (Fig. 48d, p. 122).

Neither of the median eyes of a lamprey is built well enough to have
images, or anything more than the ability to record the intensity and
perhaps the direction of light. In vertebrates higher than the lampreys,

--EPIDERMIS-^
"""■-CORIUM -'-

SUPERIOR

HABENULAR

COMMISSURE

PARIETAL NERVE

NEAL TRACT
DBRAIN
POSTERIOR COMMISSURE

NEAL TRACT

IB ANURANl

DORSAL SAC

SUPERIOR HABENULAR/

COMMISSURE

POSTERIORI
COMMISSURE

Ic. reptile]

ID mammal]

Fig. 124 — Condition of the pineal and parietal (parapineal) eyes in various vertebrates.
After Neal and Rand.

only one of these eyes is ever to be found. The stegocephalians must
have had the pineal eye at the height of its development (Fig. 61b, p,
p. 137), if we can judge from the size of the foramen for its nerve in the
stegocephalian skull. But in modern amphibians it is vestigial, in the frog
a mere cyst underlying the skin of the 'brow spot'. In birds it has gone
completely, and in mammals it has been converted into the 'pineal gland'
of dubious, possibly endocrine, function.

The parietal eye must have been somehow represented in the stego-
cephalians; for, though it is completely lacking in modern fishes and
amphibians, it is present as the sole median eye in modern reptiles. It is

340 ADAPTATIONS TO SPACE AND MOTION

functional and provided with a lens and a fairly fine-grained retina in
Sphenodon and in some lizards.

One can understand why the eventual single parietal eye of the rep-
tiles should have ceased to be an eye, and disappeared, in their avian
and mammalian descendants; for, being unprovided with lids, it could
not clear a way for its operation through the shrubbery of feathers or
hair. But a good question which has never been answered — ^perhaps never
even raised before — is : why did the median eyes ever lose their bilateral
paired condition, and why was one member of the lamprey's tandem
combination eliminated by higher forms which perfected the eyes but
kept only one of them?

This question is not of any real importance; but it is an interesting
one, and perhaps we can answer it in the light of the foregoing discus-
sion of the universal fusibility of the binocular images of the lateral eyes.
It seems quite possible that the dorsal eyes, being less fortunate in their
cormections within the brain, yielded sensory impressions which were
incapable of any sort of fusion — just as our two hands, separately and
simultaneously touching steel and leather, give us normal impressions
of those two materials and not of a single hybrid substance of inter-
mediate or summated properties.

If no fusion could be accomplished between the members of a pair of
dorsal eyes, no harm was done as long as the eyes were not capable of
seeing pictures. But as their lenses evolved and their retinae improved,
this point of perfection was reached and difficulties arose. So far as we
can tell, none of these median eyes ever had any muscles to move them,
or indeed any accessory organs of any kind. With rivalry or diplopia
occurring in each pair, the number of pairs was radically reduced to two,
and one member of each pair was discarded (Fig. 54b and c, p. 126).
When at last the eyes became such good ones that diplopia between the
unconvergible tandem eyes became intolerable, one of them had to go.
The solitary remaining median eye could then be perfected to any degree
by the ancient amphibians and early reptiles, without further diplopic
trouble or even any danger of its field of view overlapping into the fields
of the lateral eyes.

The reptilian lateral eyes are such very fine visual organs, however,
that in this group the median eye lost most of its importance. Gone in
the turtles, gone in many lizards and in all snakes, it was already well
on its way out of the vertebrate picture even before it was finally buried
beneath the plumage and fur of the birds and mammals.

MONOCULAR STEREOPSIS 341

Substitutes for Binocular Stereopsis — It would be rather hard to
say which of the possible monocular cues to distance (pp. 313-4) a given
animal can and does use. But one of these cues, the production of par-
allax by head movements, is also valuable for throwing objects into
'relief; and when an animal habitually employs this process the fact is
quite evident. A number of lateral-eyed vertebrates, whose binocular
fields are so narrow as to be practically useless, obtain a perception of
solidity and relief — a sort of monocular stereopsis — by invoking parallax
in one way or another.

When, as children, we dropped a prized penny upon a brown rug on
which it became invisible, we located it by getting down on the rug and
placing an eye close to its surface, so as to see the profile of the coin in
relief. A few years ago, Joseph Grinnell called attention to the fact that
there are many birds which do something quite comparable. Birds either
eat moving food, pursuing it or waiting for it to come along; or they
seek motionless food, such as seeds. Birds in this latter category perform
what Grinnell called 'rapid peering' : they cock the head this way and
that several times before pecking at a seed or berry, thus placing it in
relief against its background from several different angles in quick suc-
cession, and identifying and localizing it with precision before pecking
it with assurance.

The shadow cast by a solid object gives it relief, for when seen from
more than one angle either simultaneously (as in binocular vision) or
successively (as with rapid peering), different amounts of the shadow
are visible and the prominence of the object can then be evaluated.
Benner has recently shown that in the pecking of grains by chicks, the
shadow is of great importance. If the kernels were so illuminated that
their shadows were eliminated or displaced, the chicks ignored them.
Painted representations of shaded kernels deceived them, though Benner
says that they seemed aware that they were being fooled. One-eyed chicks
were as well able to peck accurately as two-eyed ones, for both used only
monocular parallax for ascertaining distances. Apart from experiments,
we have abundant evidence of the importance of shade and shadow to
animals for their perception of relief, in the form of the many dermal
camouflaging devices adopted (particularly by insects, fishes, and rep-
tiles) for obliterating shadows or for creating 'false relief through the
use of color spots graded in tone. The interested reader should consult
the work of Cott listed in the bibliography.

342 ADAPTATIONS TO SPACE AND MOTION

Some birds when walking (fowls, pigeons, doves) and others when
swimming (coots and gallinules) make perpetual forward-and-backward
oscillatory movements of the head. It has been claimed that the eyes
never actually move backward through space — the forward movement
of the body just cancels the backward movements of the head. Thus
although the body moves forward steadily, the head moves forward
through space by jerks and pauses. In effect, the eyes obtain a rapid
succession of previews of the surroundings from constantly new angles.
The forward movements of the head being so quick, each new parallac-
tic observation of the field is made almost simultaneously with the pre-
ceding one, and the exaggeration of the apparent relative motions of
objects at different distances furnishes a basis for the estimation of dis-
tance and relief.

Many shore birds bob their heads vertically as they teeter along the
beach, and many snakes weave their heads from side to side during
scrutiny. Some birds and many lizards commonly have spells of nod-
ding periodically. These habits have been interpreted as devices for
producing an artificial relative motion in the surroundings. Many herpet-
ologists believe that the nodding of lizards is a sociological phenomenon
— the animals do it most when they are among their fellows, when they
are warmed up, well-fed, when they 'feel good' and so on. But this only
means that they nod most when they are in normal condition and on
the alert. The habit does not seem to be sexual; and if it is social at all
it is still not without visual importance. If a lizard nods mostly in the
presence of other lizards, that may merely signify that for a lizard noth-
ing so much merits close scrutiny and visual cogitation as does another
lizard.

(E) Movement-Perception

Human vision is such an enormously rich complex of experiences, and
human beings are so diversified in habits and interests, that no two of us
value our eyes for quite the same set of reasons. If asked what aspect of
vision means most to them, a watchmaker may answer "acuity", a night
flier, "sensitivity", and an artist, "color." But to the animals which in-
vented the vertebrate eye, and hold the patents on most of the features
of the human model, the visual registration of movement was of the
greatest importance.

Any sense organ exists not simply to give its owner awareness of some
physical, environmental agency, but to provide a basis for awareness of

DETECTION, SALIENCY OF MOVEMENTS 343

change in the force or the substance which it records. The most impor-
tant changes in visual stimuli are changes in their locations. No sense
other than vision is at all reliable for the orientation of animals with
respect to the objects in space — bats, with their miraculous ears, again
excepted. And, the big reason why it is vital to know where things are is
that some of those things, and the animal itself, move. Indeed, if nothing
on earth moved, there would never have been such things as eyes. Plants
do not have them, and neither do sessile relatives of eyed animals — sea-
lilies and barnacles, for example.

But all vertebrates move about, even if a few, like the ectoparasitic
dwarf males of certain fishes, do not do so under their own steam.
Always, the vertebrate eye has recorded movement, regardless of the
evolutionary ups and downs of its capacities for sensitivity, acuity, and
color-reception. We can imagine vision with any of these aspects close to
the vanishing point, but not vision without awareness of motion. Psy-
chologists are fond of pointing out that a wiggling finger, seen in the
extreme periphery of the visual field, is not seen as a finger with a certain
brightness, color, and form, but is perceived as pure, disembodied wiggle.
Vision in the periphery being crude and 'primitive', the conclusion is
often drawn that motion is just about the most ancient and primitive
aspect of vision. Motion may persist when all else is lost — an individual
with a large scotoma or with hemianopia (v.s.) may see the motion of
objects (though not the objects) in what is otherwise a completely blind
field.

Detection versus Saliency — If the biological need for a capacity to
perceive movement varies from animal to animal — and it obviously does
— we may reasonably look for diflFerences in this capacity. But although
we may be able to see morphological and physiological differences which
should affect the movement-seeing capacity, we cannot very well assay
another set of factors which is of enormous importance. These are the
psychic factors which have to do with the conspicuousness in con-
sciousness, the saliency, of movements — with their 'attention-value' and
importance to the animal, in other words. Animal A may have a far
poorer objective basis for detecting movements than species B; yet we
may find that species A gives a violent reaction of fear or flight to a slight
motion in its surroundings, while animal B calmly contemplates moving
objects without making any overt response to them. Here, we can attempt
to evaluate only the most nearly objective factors in movement-percep-
tion. The subjective factors which endow motion-percepts with their

344 ADAPTATIONS TO SPACE AND MOTION

greater or lesser saliency must go largely undiscussed since we know so
very little about them in man, and still less about them in the other
animals.

Naturally, there is a rough correlation of saliency with feeding habits.
The well-armed carnivore does not need to be so fearful of unidentified
moving objects as does a timid and defenseless herbivore. For, in wild
nature, a moving object is generally another animal, and the observer's
responsiveness to it will depend upon the importance, to him, of reacting
in a motor way to another animal's approach.

Movement may thus have unequal attention value and exciting power
for animals whose apparent objective basis for detecting movements is
about the same. Or, animals with vastly different eyes may respond to
moving and motionless objects in very similar ways. For instance, a frog
will snap only at small moving objects — which, in his natural surround-
ings, are ordinarily things which are good food for him. A penguin will
seize and eat only living, moving fishes. Though the penguin's visual
capacities (including those which we think have a bearing upon the detec-
tibility of movements) are vastly different from the frog's, either animal
could be perched on a mound of its natural food, fresh-killed, and would
proceed to sit there and starve to death. Such is the power of moving
matter over animal minds.

In general, the less well developed the area centralis or fovea, the
more dependent is the animal upon the movements of objects for their
detection and evaluation. The penguin is probably an exception —
he sees a motionless fish well enough, but instinct tells him that a dead
(i.e., motionless) fish is not good to eat; and his olfaction, as in all
birds, is too poor to differentiate fresh-killed fish from stinking carrion.
Lacking sharp vision, an animal not only misses many sidewise move-
ments, but is readily stalked by an enemy which is careful to approach
in a straight line. Recognition of such toward-movements depends upon
appreciation of the 'growth' of the retinal image — which is poor where
acuity is low, both for direct reasons and also because poor accommo-
dation always accompanies poor resolving power.

Not only amphibians, but most snakes, lizards, and many carnivorous
turtles appear not to see motionless prey. Motion is particularly impor-
tant to diurnal snakes, whose visual acuity is probably the lowest of any
diurnal vertebrates — Dryophis being a conspicuous exception in its abil-
ity to secure motionless prey solely by sight. Other diurnal snakes 'lose
contact' with the prey if it stops moving or freezes, and then attempt to

GRADES OF MOVEMENT 345

regain rapport through olfactory exploring or trial-and-error tonguing.
Nocturnal snakes, many of which have superb olfactory powers, are
better able to locate and strike motionless prey, without need of vision.

Though all birds have high visual acuity, hawks and insectivorous
forms are dependent upon motion for seeing prey at great distances. The
bird sitting on a fence-post may fly suddenly and directly to a point rods
away, pick up an insect, and return. This is a marvellous ability; but we
should not credit the bird with distinguishing a motionless bug at such
distances. In all probability the bug was moving or the bird would not
have seen it; and this is not entirely a matter of the saliency of the move-
ment, for, as will be brought out later, the same object can be distin-
guished about twice as far away, if it is in motion, as when it is still.

Mammals in general are also quite dependent upon motion. The suc-
cessful use of the habit of 'freezing' by rodents and ungulates is in itself
an evidence that the carnivores which prey on them do not identify them
visually when they are still. Two or three breeds of dogs — the borzoi, the
greyhound, and to a less extent the dachshund — hunt by sight and must
keep the prey in sight or give up the chase; but such a situation is rather
artificial for a carnivore and is to be laid to the effects of breeding. Small-
eyed, nocturnal mammals are particularly dependent upon the move-
ments of their enemies for apprisal and escape. As we shall see, the eyes
of such animals as rats and mice have been called adapted to see motion;
but the truth is that they see motion better than form and color only by
a process of elimination — they are simply not good enough to see any-
thing except the gross movements of large objects.

Grades of Movement — The most obvious basis upon which we might
classify movements is their speed. But speed is entirely relative, and is
related to the animal's own speed of movement. What may seem very
slow to a rabbit, may seem whizzingly fast to a snail. Obviously, the same
sensory and perceptual machinery is set in motion whether an object
moves past an animal or the animal moves past the object. What occurs
is a relative change of position of the two, and the animal's capacity for
maintaining a clear impression of an object must be adequate to cover
the speeds attained by natural objects important to him, as well as his
own locomotor speed among such objects when the latter are motionless.
The speed at which it is safe for an animal or a man to travel is largely
determined by his reaction time; but it is obviously not safe for an animal
to be unable to see an approaching enemy as anything more than a blur.

346 ADAPTATIONS TO SPACE AND MOTION

unless he can easily outrun that enemy. We may be sure that any animal
can see, as clearly as if it were motionless, any object moving as fast or
somewhat faster than the animal himself can go. It will be recalled that,
other things being equal, the size of an animal's eyes is related to his
speed of locomotion (Leuckart's ratio). Bearing in mind that visual
acuity tends to rise with eye size (see p. 171), we shall shortly see why
this should be.

Some objects move too slowly or too fast for any motion to be seen.
Suppose we consider only perceptible movements, and separate them into
slow, medium, and fast. The ranges of absolute speeds embraced by
these terms will vary from species to species and, of course, with the dis-
tance of the moving object from the observer. Let us call 'slow' all move-
ments during which the character and details of the object are as clearly
seen as when the object is still. There will be even slower movements
which will not be seen at all. When we watch the minute-hand of a clock,
for example, we are aware from time to time that it has taken a new posi-
tion; but we cannot honestly say that we see it move. Let us coin a term
and say that the movement of the clock hand is for us, psychologically,
infra-perceptible.

The fastest movements we can detect are those in which we are unable
to detect direction. An object can flit so rapidly across the whole visual
field that we are unable to say whether it went from right to left or from
left to right. Here, we do perceive motion, but not a movement at a cer-
tain rate over a certain distance. Still faster objective movements may be
supra-perceptible, where the speed is so high that nothing is seen at all.

By elimination, 'medium' movements are those in which not only a
change of the position of an object can be detected, but also the changing
of position. The nature of the moving object can be made out more or
less well. It is with the perception of medium movements that we are
most concerned. The whole percept of such a movement may be
described as a comet, whose head is the object and whose tail is a blur
which we interpret as 'movingness'. When a cartoonist suggests motion
by putting a series of partial outlines behind an object, he has wrought,
better than he knows, a realistic diagram of movingness as a train of
overlapped after-images.

So, objective movements may be :

A. Infra-perceptible — so slow that only a change of position is noted
from time to time.

RELATIVITY OF MOVEMENT-PERCEPTION 347

B. Perceptible as :

1. Slow — where the percept is, so to say, all object and no blur.

2. Medium — where the percept is comet-like, the object being
seen with a tail of blur, or 'movingness'.

3. Fast — where the percept is all blur and no object, with direc-
tion difficult or impossible to decide.

C. Supra-perceptible — so fast that nothing is seen at all.

All of these definitions, it is understood, concern movements of objects
which are not being followed or 'pursued' by the eyes. Where voluntary
pursuit eye movements occur, all rules are off with regard to the changes
of the appearance of the moving object with changes in its speed. The
object may be seen as clearly as if motionless, if the pursuit movements
are precise enough to hold its image on the fovea. But even though this
image does not move over the retina, the images of background objects
do so move, and their apparent speed of movement helps us to gauge
the speed of the moving object.

The Relativity of Movement-Perception — Relative movement of
the object and its background is essential for any accurate perception of
slow motions. In a darkroom, a single spot of light may be motionless
and yet appear to be moving, or moving and appear to be motionless;
for, eye movements of which we are unaware are then taking place and
the shift of the image of the spot over the retina is misinterpreted. This
is the explanation of the 'autokinetic movement' of a stationary spot of
light which we attempt to fixate, and think we are fixating, but which
seems to wander here and there over a considerable range. If two lights
are presented and only one is moved, we may see both as moving if they
are alike; but if one is larger or brighter than the other it tends to take
on the attributes of a 'ground' and we see the other light as moving even
though it may be the one which is actually stationary. For us to be sure
that an object is moving, it is ordinarily necessary that we be able to see
some other object which we know or believe to be stationary. In fact the
more other, motionless objects we can see, the better for our accuracy in
detecting the direction and extent of a motion. The minimal angular
velocity for our perception of motion is only one or two minutes of arc
per second of time when there are stationary objects in the field; but
when there are no such objects to serve as landmarks, the velocity of the
moving object must be made ten to twenty times as great. The local
signs of direction, and of change of direction, in our retinae work well

348 ADAPTATIONS TO SPACE AND MOTION

only in a visual field which has pattern. The perception of a real move-
ment does not depend solely upon a displacement of an image on the
retina, but upon a displacement relative to the images of other objects.
Visual orientation in space becomes as imperfect as auditory, as soon as
visual space is greatly emptied of reference-objects.

Motor Factors in Movement-Detection — It might seem that all of
the 'objective' factors in movement perception should be purely sensory,
but there are certain ones which are chiefly motor in character — notably,
the 'gyroscopic' action of the involuntary eye movements, under the con-
trol of the membranous labyrinth. This action tends to preserve the abso-
lute orientation of the eyeball in space so that — as Erich Sachs puts it —
"the head rotates around the eye" during the dynamic maintenance of
equilibrium. This maintenance of ocular orientation makes toward a con-
stancy of the visual field, whereas voluntary eye movements are designed
to exchange the field and fixation-point for new ones.

If the eyes always turned with the head instead of automatically
'against' the head, the swimming of the visual field in a wholesale 'appar-
ent movement' would conceal from the animal small real movements
within the field. So many more parallactic relative movements would
take place, that actually-moving objects would be harder to spot. The
gyroscopic stabilization of the eye is a means of combatting the rela-
tivity of motion — by keeping the visual field still, the animal can better
know what moves, when, and where.

Another motor phenomenon whose sensory accompaniments aid in
movement-detection is the 'saccadic' eye movement. This is the type of
voluntary eye movement which we make to change our point of fixation.
During involuntary movement of the eyes, and during pursuit move-
ments, we see continuously. But it is a striking fact, more than a little
hard to believe, that we do not see at all during saccadic movements.
Some sort of switch is opened in the brain, until the movement is com-
pleted. Then, vision returns. One simple proof of this is the fact that it
is impossible to see the eyes in voluntary motion in a mirror. Another is
Dodge's experiment: look at an object through the narrow apex of a
paper cone, then look to one side of the aperture and sweep the line of
sight across it. You will see nothing of the object, through the aperture,
unless the line of sight stops upon it. We read a line of print not con-
tinuously but by jerks, seeing the words only in the moments when the
eye is at rest. The fewer stops one makes per line, the faster a reader he

FACTORS IN MOVEMENT-DETECTION 349

can be; and yet, the fewer stops one makes, the more time one is actually
seeing the words.

If one holds the eyes motionless in the orbits and turns the head from
side to side, vision is then continuous and one experiences the same
'swimming', or apparent movement of the whole field, that occurs during
vertigo or intoxication when the reflex eye movements (during which
vision is also continuous) are occurring in such an abnormal way that
the 'gyroscope' is wobbly. But now if the head be kept still, and the eyes
swept voluntarily from side to side through the same angle as before, the
field does not swim because vision occurs only at the multiple stopping-
points of the eye's discontinuous rotation.

Here again, in the suppression of vision during saccadic eye move-
ments, we have a mechanism for maintaining a constancy of the direction
of objects, so that if one of these should move, we will be better able to
notice it. There seems to be no other reason why this kind of 'suppres-
sion' ever evolved. The chances are that in some animals whose eyes
move but Uttle or not at all, a similar suppression takes place during head
movements, such as the perpetual fore-and-aft movement of a walking
pigeon's head.

Beebe describes an experience he has had, while helmet-diving in
shallow water, which demonstrates strikingly the relativity of movement
for animals and their dependence upon a constant visual field for the
recognition of movements. The movements of the water were causing
the bottom vegetation to sway slowly to and fro. As long as Beebe
swayed his body with the plants, the many fish in the neighborhood
ignored his presence. But when he stood erect and motionless, the fish
were immediately curious about him and came over to investigate.

Sensory Factors in Movement-Detection — Given a situation in
which the background and motor factors are conducive to the perception
of a movement, and do not tend to conceal it among apparent move-
ments or to create a 'referred' movement (i.e., cause the motion to be
attributed to the wrong object), there are two principal sensory fartors
which come into play. These are visual acuity and the persistence-time.
It is upon the value of each of these, in a given animal, that the demar-
cations between imperceptible and slow, medium, and fast perceptible
movements will establish themselves for that kind of animal.

The dependence of movement perception upon visual acuity does not
at first glance seem to be very direct. We can see an object, if it is in

350 ADAPTATIONS TO SPACE AND MOTION

motion, from a much greater distance than that from which we can
resolve it if it is still. Ovio has given a simple explanation of this : If we
take as our criterion of visual acuity the two-point limen, or angular
separation which two points must have if they are to be just resolvable
as separate points, then their subjective separateness is due to the fact
that their images on the retina fall upon 'circles of innervation', or groups
of visual cells (one in each 'group', in the fovea) connected with single
optic nerve fibers, which have between them an unstimulated circle of
innervation. The actual separation of the points in space thus corres-
ponds, in the retinal image, to the diameter of a circle of innervation in
that part of the retina. But now if the displacement of a single point in
space is to be visible, the image of that point need move on the retina
a distance equal only to the radius of a circle of innervation, in order to
fall upon a new circle and register the displacement.

This idea is quite well borne out by the experimental facts. The two-
point limen at the human fovea is about 40" of arc. The angular dis-
placement-threshold at the fovea is 20" of arc or less, according to dif-
ferent observers. Schmid, studying the visual performance of fourteen
police dogs, found that the best dogs could recognize moving objects at
810-900 meters, while the best record with the object stationary was
585 meters — not far from the 2 : 1 ratio which Ovio's explanation roughly
predicts. Thus, paradoxically, it seems that we should, after all, discrim-
inate changes in a visual pattern better than the static features of the
pattern itself.

When a visual stimulus is presented, there is a 'latent period' before
the sensation develops, and the sensation lasts longer than the presen-
tation-time or duration of the stimulus. The 'persistence time' is the
period within which a stimulus continues to be sensed after it has been
removed. In vision, this period is synonymous with the duration of the
'immediate positive after-image' of a stimulus. It is commonly stated to
be responsible for making motion pictures 'move', though it is directly
involved only in the elimination of 'flicker' from them. If an after-image
has not commenced to fade before an identical second stimulus evokes
its full-strength sensation, the second sensation or impression will merge
with the first. As successive flashes of light are thrown on the same ret-
inal area, an increase in their frequency leads ultimately to the percep-
tion of a steadily-burning light, at the 'critical frequency of fusion'.

Now, at this critical frequency, the interval between the cessation of
one stimulus and the commencement of the next might be called a

FACTORS IN MOVEMENT-DETECTION 351

'refractory period', because no identical stimulus presented within this
period can be perceived as separate from the preceding one. The period
has been called by von Uexkiill the 'biological moment' — the shortest
discriminable unit of time for the animal. This name for it has justifica-
tion only if it be found that in all sensory modalities the duration of the
'moment' is about the same. And, Uexkiill did find very good agree-
ment. Thus for example, a snail fuses visual impressions coming at four
or five per second, and cannot distinguish mechanical taps on its foot,
at this same frequency, from a steady pressure. We fuse movie frames
at 16 per second, and the lowest frequency of auditory impulses which
we fuse into a steady tone is also 16 per second. But, with each of the
senses, the duration of the 'moment' is profoundly influenced both by the
intensity of the stimulus and the adaptation-condition of the sense-organ.

We can now understand how the persistence time affects the percep-
tion of movements at different speeds. As an object moves slowly across
the field we see it with the same clarity, at each instant, that we would
if its image were motionless upon the part of the retina which it strikes
at that instant. The after-images of the object are being given adequate
time in which to fade. With increasing speed, the image of the object in
a given position is overlapped by, and blurred by, the after-images of the
object in its just-previous positions. We see this blur as movingness and,
if the visual acuity of the particular retinal area is extremely low, the
movingness may seem disembodied. If, now, the object traverses the en-
tire field within the period of the persistence time, we will obviously see
nothing but blur, and perhaps cannot decide the direction of the move-
ment. And, if the object is of such brightness, and moves at such speed,
that its image endures for too short a time on any one spot of retina to
arouse any sensation, the flight of the object — a bullet, for instance —
becomes supra-perceptible. But by enlarging or brightening the object
(as with a howitzer shell, or a tracer bullet) we may restore visibility of
its flight even at terrific speed.

A few years ago, quite a furore was created by the scientific announce-
ment that a deer-fly can travel at 800 miles per hour. Skepticism took
various forms. A biochemist computed that the fly would consume its
own weight in food every hundred yards or so at such a level of muscular
activity. Langmuir, of the General Electric Company, noting that the
deer-fly at its speediest is still visible, swung a fly-sized lead pellet at the
end of a wire at known speeds. When the linear speed of the pellet was
13 miles per hour, the pellet was blurred. At 26 miles per hour it was

352 ADAPTATIONS TO SPACE AND MOTION

barely visible as a moving object. At 43, it became a faint line whose
direction could not be recognized; and at 64 miles per hour it was wholly
invisible.

It is sometimes given, as a characteristic of true movement perception,
that we do not see the object in all of its intermediate positions. That
really depends upon the nature of the object. The body of an automo-
bile may be seen clearly at all points in a movement at a given speed.
But the tops of the wheels are travelling faster than the car itself, and
so the wheels may blur. Before the invention of the motion-picture
camera, a famous photographer, Eadweard Muybridge, made photo-
graphic studies of the gait of running horses at the behest of a group
of sportsmen who wanted to settle an argument as to whether a trotting
horse ever has all four feet off the ground at once. Muybridge used as
many as forty automatic cameras spaced along the track. When some
of his pictures were handed to horsemen, they refused to believe that a
horse's legs ever get into some of the positions shown in the photos.
But they were forgetting that while the horse's body cannot travel too
fast to be seen clearly, its legs in their forward movements travel so
much faster than the horse that they blur in human vision, and no one
can honestly say that he sees them in all their positions. While the eye
is following the horse's body by a pursuit movement, it cannot very well
follow, at the same time, the movements of the horse's legs.

Adaptation, and Center versus Periphery — The higher the visual
acuity, the lower the angular displacement threshold — hence, the better
a moving object can be seen and the smaller a movement can be detected.
The higher the critical frequency for fusion, the shorter the persistence
time (and, sometimes, the latent period) — hence, the less the blur of a
moving object and the faster it can move and still be seen well as to its
nature, direction, and velocity.

Visual acuity and critical frequency, being fairly easy to determine
in man and animals, are thus our best criteria of the comparative objec-
tive capacities of vertebrates for movement-perception. But both of these
values are very different for the cone-mechanism and rod-mechanism of
the retina. In the average retina (one which is duplex and has an area
centralis) both values are profoundly influenced by the conditions of
light- and dark-adaptation and by the differing concentration of rods
and cones in the center of the retina as contrasted with the periphery.

It is generally believed that movements are better seen peripherally
than centrally. The situation with regard to the objective {i.e., physi-

ADAPTATION; CENTER VS. PERIPHERY 353

ological) factors does not bear this out. But the psychic factors are
largely in favor of the periphery, in which movements have a saliency
and attention-value quite out of proportion to the clarity with which
they are actually discriminated. We might think that this was a com-
pensation for the inferior capacity of the periphery to detect movements;
but a moment's reflection shows that there could be no such compensa-
tion, any more than increasing the strength of our brightness-sensations
could of itself make the eye more sensitive to weaker lights.

So, when the retinal* periphery is described as "an organ which is
specially adapted to see movement", we need to append: "so far as
psychic factors are concerned." Animals with panoramic vision, animals
which like the horse have greatly extended peripheries and wide visual
angles, and animals like the mouse with pure-rod retinae (which can be
thought of as 'all periphery') , are not specially equipped to discriminate
movement and moving objects. If in the rat's whole retina, or in the
ungulate's periphery, visual acuity is so low that only movingness, not
moving objects, can be seen, it is not that these retinal areas are designed
for movement-perception — rather, it is that they are too crude to afford
any phases of vision except movingness and brightness. What move-
ments the animal does pick up may startle him more than they would a
lizard or a man; but this is a matter of saliency, the biological need or
lack of need for which varies from species to species. Lizards and men
are better able to identify a moving object promptly, and are therefore
not under the necessity of treating every moving object which enters the
visual field as a dangerous enemy until it proves itself otherwise.

Certainly, as Woodworth says, the brain is tuned to see motion and
grasps at any chance to see it. That is doubly true when the brain is
peering out at the world through the periphery of the retina. Even the
momentary stimulation of the periphery by a spot of light is said to
cause an impression of movement. A moving point in the periphery is
more visible than a line of similar length, direction, and duration. There
are two factors which operate to promote movement-detection in the
periphery. One of these is quite important, and gives a moving object
a sort of physiological saliency which may indeed be a large part of the
basis of psychic saliency. This is the great 'fatigibility' of the periphery.
Motionless objects in the periphery of the visual field actually tend, from
this cause, to disappear after a few moments. But now if one of them
begins to move, it is immediately seen again, since its image passes over
retinal areas which have meanwhile become adapted to other images but

354 ADAPTATIONS TO SPACE AND MOTION

are responsive to any change. Another, and minor, advantage of the
periphery which depends upon the morphology of the eye (actually,
upon one of its so-called imperfections) is the 'barrel distortion' of the
peripheral field: as a circular image swings steadily outwards along a
meridian of the retina into the far periphery, it becomes elUptical with
its long axis meridionally oriented. If two such images move together
into the periphery, hailing from two objects whose separation in space
remains constant, the distance between the images (hence, the disparity
between their apparent relative speeds) incre^es along with the dis-
tortion. We may not be conscious of any peripheral aberration of shapes
under ordinary conditions; but nevertheless peripheral movements, in
meridional directions at least, are optically exaggerated to a not unim-
portant degree by this increased speed of the sweep of the image over
the retina. In some animals' eyes, where the retina is broadened in the
horizontal meridian by an ellipticity of the eyeball (horse, swift fishes) ,
this factor may be quite important.

Many more factors, however, operate to the disadvantage of the
periphery in movement-detection. Foremost of these is the rapid fall of
visual acuity from center to periphery, which is an expression of the
increasing size, meridionally outward, of the circles of innervation. The
acuity of displacement-discrimination also falls from center to periph-
ery, though not as rapidly as does the resolving power. In light-adapt-
ation, when central (i.e., cone) vision is at its best, the central fusion-
frequency is higher than in dark-adaptation; and, of course, visual acuity
also rises with intensity. In dark-adaptation, where the rods are under
optimal conditions, acuity is low; but it so happens that the peripheral
critical frequency is higher than it is in light-adaptation. In a duplex
retina under any given adaptation-condition, the central acuity and
critical frequency are ordinarily higher than the corresponding peripheral
values. The higher the illumination, the farther peripherally a movement
of a given speed is appreciated, due to the cones coming into play.
When the periphery is dark-adapted, however, it may still record flicker
when this has disappeared for a partly light-adapted center. One can
experience this at the movies, where the screen is flickerless but a hand
moved across the lap (while the screen is fixated) is seen intermittently.

Similarly, rod-rich retinae (cat, owl) have been found to have lower
critical frequencies than cone-rich ones (pigeon) in the same condition of
adaptation. We cannot compare with perfect fairness the light-adapted
central vision and dark-adapted peripheral vision of a duplex retina with,

ADAPTATION; CENTER VS. PERIPHERY 355

respectively, pure-cone and pure-rod retinae under their respective optimal
conditions; for there are mysterious mutual inhibitory effects of the rod-
and cone-mechanisms of a duplex retina. But, from the data on critical
frequencies at least, we may suggest that a diurnal animal has his best
movement-perception in the daytime while a more rod-rich, nocturnal,
animal sees movements better at night than by day. In pure or simplex
retinae, acuity-differences between the light-adapted and dark-adapted
conditions are probably slight as compared with the differences in visual
acuity between light-adapted duplex retinae and dark-adapted ones; so, in
both pure-cone and pure-rod animals, the adaptation-state probably influ-
ences movement-perception chiefly through its effect on fusion-frequency.
When both diurnal and nocturnal animals are adapted to the same
illumination however, we should expect the movement-perception of the
diurnal form to be always superior on the grounds of both the visual
acuity and persistence-time factors.

Other factors militating against the periphery are its poor perform-
ances in the matter of discriminating hues and the discrimination of
intensities. Both of these capacities are involved in visual acuity in its
broad sense — that is, in the perception of pattern, and consequently of
the changes of pattern which result from movements. Farther and farther
peripherally, fewer and fewer hues, less and less saturated, are seen.
At least, this is true of man, and probably of all color-perceptive verte-
brates. And, the discrimination of intensities (and hence, of contours
between areas of different objective limiinosity) is much poorer periph-
erally than centrally, and poorer in dark-adaptation than in light-adap-
tation. As a consequence, it is found that movements are perceived
farther into the periphery, and more easily, when the background is
made brighter to give the object more contrast.

Wavelength as such can also influence movement-perception, presum-
ably even in animals which have no color vision; for the critical fre-
quency differs for different hues of light. A Swedish railroad recently
found that certain red signals, which had to be seen as blinking, could
be so seen if they flashed 75 times per minute. Blue ones could be
allowed to flash only 20 times per minute, else there was danger of
fusion by the dark-adapted eye of the engineer.

We cannot say very much about the basis of the saliency of move-
ments, even in human vision. The apparent rate of a movement is almost
twice as great if some stationary object is fixated, as when a moving
object is pursued by the eye. Probably this is due to the fact that in the

356 ADAPTATIONS TO SPACE AND MOTION

first case the blur of movingness is attached to the object, while in
the second case the object is clearer — therefore less 'moving'; and also
the blur of the shifting background, being out of focus to begin with
(since the eye is accommodating for the object) is less prominent in
consciousness. Still, even with steady fixation, movements seem two or
three times as fast when seen peripherally as they do in direct vision.

Not all perceptual factors promote saliency, however — some have a
reverse effect. If two lights are flashed simultaneously just once, one
being seen centrally and the other peripherally, they appear to flash in
succession with the central light leading the other. The latent period of
perception is thus longer in the periphery. A French worker has studied
the whole sensorimotor reaction time with central versus peripheral vision
and with the motor elements constant. A chronoscope was used, whose
indicating hand could be started moving by the experimenter and stopped
by the subject's pressing a key as soon as he was aware of the movement.
On the average, the whole reaction time with central observation was
0.170 seconds, while at 90° in the periphery it was extended to 0.327
seconds. This means that an object would have time to move farther in
the periphery, as compared with the center of the field, before the
individual could take any motor action upon the matter.

On the whole, it would seem that the periphery exercises its greatest
usefulness in movement-perception by instigating the reflex 'eye-jump'
which calls the visual axis over to aim at the locus of the movement.
This reflex is very strong, even in civilized man, who should theoretically
have very few primitive fear-reflexes left. It may not occur when the
peripheral movements are expected or at least not unexpected; but a
man in strange surroundings will inevitably turn his eyes — the first time,
at least — to see foveally a waving window-curtain or what not, which
has 'caught his eye' peripherally.

Stroboscopic Movement versus Real Movement — There are many
kinds of apparent movements — perceptions of movement where the ob-
ject to which the motion is attributed is actually stationary. Most of
these have their basis in movements of the eyes, or of the head, of which
the subject is unaware — the visual axis swinging, though the subject
believes his fixation to be constant. Any disturbance of egocentric local-
ization, as in vertigo and intoxication, results in a swimming apparent
movement of the whole field. In another category are after-images of
motion, where both the eye and the apparently moving object are station-

STROBOSCOPIC VS. REAL MOVEMENT 357

ary. One experiences this illusion after watching a waterfall or a stream
for a time, and then turning one's attention to objects on the bank.

The third, most important and most interesting kind of apparent
movement is that called variously stroboscopic or cinematoscopic move-
ment, or the '^-phenomenon'. It is obtained either when identical or
slightly differing images fall in succession upon neighboring retinal
areas, or when slightly different images fall successively on the same
retinal spot.

The stroboscope (meaning 'whirling looker') was invented almost
simultaneously by Plateau and Stampfer more than a century ago. In
any of its many forms, it is a device for making moving objects appear
to be stationary, where the object — usually a rotating one — has a regular
and serially-repeated pattern. The reader can make a simple stroboscope
(see Fig. 125a) in the following way: Take a disc of cardboard about

Fig. 125 — Simple stroboscopes (see text).

eight inches in diameter and puncture its center with a pencil which can
then serve as an axle. Draw a few radial pencil lines on the disc, evenly
spaced. Punch small holes through or between these radii, equal in
number to the latter, equally spaced apart, and equidistant from the
center. Now place the disc with the pencilled radii facing a mirror, and,
with the eye looking into the mirror through one of the small holes,
spin the disc.

One sees the pattern of pencil lines 'standing still', like the spokes of
a motionless wheel, no matter what the speed of the disc. The eye sees
the group of lines reflected in the mirror every time a hole comes along,
but the small hole permits such a brief glimpse that no motion of the
lines is perceptible. Since, through each hole, lines are always to be seen
pointing in the same set of directions, only this single changeless pattern
can be seen.

358 ADAPTATIONS TO SPACE AND MOTION

The higher the speed, the smaller the holes must be to 'stop' the
motion, until impracticably small holes are required. In stroboscopy in
industry, for seeing the distortions of rapidly rotating parts, intermittent
illumination is more feasible. If a motor armature is whirling at ten
thousand revolutions per minute, and is illuminated by ten thousand
light-flashes per minute, each of very short duration, the armature is
seen as if standing still; but any distortions produced by its rotation are
visible and can be studied deliberately.

Now, if our cardboard disc should have one or two more evenly-
spaced radii than the number of evenly-spaced holes (Fig. 125b), the
pencilled pattern will appear to rotate slowly forward. If the number of
holes is in excess (Fig. 125c), the spokes will seem to turn slowly back-
ward. These apparent movements of a pattern which (seen through any
one small hole) is always actually motionless, are stroboscopic apparent
movements.

We can duplicate the essentials of this illusion in a darkroom with a
pair of small lights. If the two lights are a given distance apart and of
a given intensity, and are flashed in succession, there will be found a
time-interval of flashing at which one sees the first light apparently slide
over into the position of the second. Between the two end positions of
this 'single' light, a distinct blur of movingness is seen.

If the time interval between the two flashes is too long, however, one
sees two lights flashing in sequence with no illusion of movement. This
is called the 'successive phase' of the illusion. Shortening the time
interval now brings back the optimal phase, in which the movement is
perceived. With very short time intervals, the 'simultaneous phase' is
reached, in which the two lights appear to flash together.

This illusion is called the ^-phenomenon. The movement seen need
not be in a straight line — it always follows a course which it might be
'expected' to do. Thus, if the two stimulus-spots are both tangent to a
visible curved line, the first spot seems actually to roll along the curve
to reach the position of the second stimulus. If the two stimuli are lines
which, if presented simultaneously, would form a right angle, the appear-
ance seen in the optimal phase is of a single line pivoted at one end and
swinging through a right angle (Fig. 126).

The ^-phenomenon sounds academic when thus described in terms of
unfamiliar apparatus, but we experience it about 200,000 times whenever
we sit through a movie show. It is the (^-phenomenon which makes the
movies move, for the motion picture camera is like our stroboscope with

STROBOSCOPIC VS. REAL MOVEMENT 359

fewer holes than spokes. Each time the shutter opens to expose a frame
on the momentarily motionless film, the objects in the field are in new
positions, displaced a bit from their previous ones at the last opening of
the shutter 1/20 of a second or so ago. Projected at the same frequency
of frames-per-second, the spatial intervals between the successive posi-
tions of the screen images are filled in subjectively with the same moving-
ness we experience with our pair of flashing lights.

The ^-phenomenon is closely related to the perception of real move-
ment, but the two are not identical psychological processes. Rather, they
are children of the same mother, whose name is persistence time. To have
the optimal phase of the ^-phenomenon with, say, our two lights, the
second stimulus must appear at about the same instant that the impres-
sion of the first fades. If the second stimulus comes late, the successive

0-

Fig. 126 — Versions of the phi-phenomenon.

a, the simplest situation: when stimulus s is presented, then /, the subjert sees s apparently
move over into the position of /. b, if, in order actually to move to the position of /,
s would have to follow a curve, then the apparent movement of s will be seen by the subiea
to take the appropriate curved course, c, if, in order actually to move to the position or /,
s would have to pivot, then in its apparent movement it is perceived as doing so.

phase supervenes; and, if the second stimulus comes too soon, the simul-
taneous phase sets in. Harking back to our classification of the percep-
tions of real movements (pp. 346-7) and the influence of the persistence
time upon them, it is easy to see that slow movements correspond to the
successive phase, medium movements to the optimal phase, and fast
movements to the simultaneous phase of the 0-phenomenon.

This common dependence of movingness, in both real and stroboscopic
movements, upon the critical frequency of fusion has led to two beliefs.
Cermak once pointed out that if the two lights in the ^-phenomenon were
alternated in the optimal phase, and the distance between them reduced
to zero, one would have a single flickering light. With the rate of alter-
nation then raised to correspond to the simultaneous phase, the two

360 ADAPTATIONS TO SPACE AND MOTION

lights at zero distance would fuse into a single steady light. Many work-
ers have drawn the conclusion that our mechanism for apparent-move-
ment perception may be the only one we have with which to perceive
real movement. The 'laws of Korte', which express the interrelations of
the time interval, spatial separation, and intensity of stimuli for the
optimal ^-phenomenon, also hold very well for the perception of real
movements. That is, if a third light of the same intensity is really moved,
within the same time, parallel to the two lights used for the ^-phenome-
non, the real and apparent movements are seen alike. Speeded up to the
short interval of the simultaneous phase, the real movement becomes a
line of light without direction. Slowed down to simulate the successive
phase, the really-moving light loses its blur of movingness.

Another common belief is that the movement of the movies is solely
created by projection at the speed of the critical frequency. Since both
the elimination of flicker and the optimal ^-phenomenon depend upon
this speed of projection, the conclusion that they are identical seems plaus-
ible. But it is easily possible to separate the conditions for the optimal
(^-phenomenon from the conditions for the elimination of flicker. Sup-
pose we print every twentieth frame of the negative on successive frames
of a positive film, and project it at the usual speed. There will be no
flicker — but the spatial separations in the images will be so great that
only jerky movements or successively new positions, with no smooth
movingness, will be seen.

We need not produce such a film intentionally. It happened as an
unfortunate accident in the making of Walt Disney's Snow-White and
the Seven Dwarfs. The slow movements of the human characters seemed
unpleasantly jerky on the screen. The faster movements of the little
animals were just as jerky, but were quite acceptable to the onlooker; for
when we watch a real chipmunk skip about we do not actually see him
when he is in motion. Human movements are so much slower that the
loss of movingness, due to too great spatial separation of the successive
drawings of the animation, was 'unnatural'. Disney pushed the ^-phe-
nomenon a little too far; and to obtain any more satisfactory illusion of
human movements in animated cartoons, it is absolutely necessary to
draw just as many intermediate stages in each movement as there would
be on a motion-picture film of an actual human movement of the same
speed. While watching any ordinary movie, one can hold a finger in
front of the eyes and sweep it across the angle subtended by the screen
much faster than an object of the same apparent size would ever move

STROBOSCOPIC VS. REAL MOVEMENT 361

across the field of the camera. When this is done, the finger is seen to
jerk across the screen, taking twenty new positions per second, and does
not appear to be in motion at all.

Before we leave the movies, it is worth-while to point out that the 0-phe-
nomenon can be seen binocularly. A real movement appears just as con-
tinuous if we blink our eyes alternately while observing it. So also, the
^-phenomenon occurs if each eye sees only one of the stimuli. A movie
will still move even if shutters placed before the two eyes are opened and
closed alternately in synchrony with the alternate frames of the film —
it is only necessary to take and project the picture at twice-normal speed,
to prevent flicker. This phenomenon is the basis of some methods of
making stereoscopic motion pictures.

A common illustration of the 0-phenomenon, often suggested in psy-
chological text books because it requires no apparatus and is therefore
'simple', is actually of the binocular type — with special complications:
if a finger is held still before the eyes, and the eyes are blinked alter-
nately, the finger is seen to move from side to side. Actually, the single
finger cannot represent our pair of 0-phenomenon lights — it appears in
two positions, to begin with, only if we are accommodating beyond it.
The two diplopic images of the finger then have different apparent posi-
tions because of their different parallaxes with background objects. If
one accommodates and converges steadily upon the finger, it will not
'move' at all when the eyes are alternated. Blinking the eyes makes it
difficult to maintain the convergence for the finger. Try propping up a
pencil instead, and occluding the eyes alternately with your hands, held
before them, while watching the pencil. The pencil will not 'move', un-
less you fixate something beyond it.

Now, can the machinery with which we see real movements be, actu-
ally, our machinery for stroboscopic perception? When the distance and
duration of real and apparent movements is objectively the same, they
appear equally moving; but the real movement may seem slower and
smoother and the apparent movement a bit jerky. This jerkiness we can
attribute to the fact that the impact of the second stimulus upon its
retinal spot is sudden. The relative retardation of the real movement is
perhaps due to the circumstance that intermediate retinal areas are actu-
ally receiving stimulation; for, as is well-known, we see an occupied space
as longer than an unoccupied one, and if a movement traverses the two
in the same time, it will seem to traverse the occupied space more slowly.

362 ADAPTATIONS TO SPACE AND MOTION

But there is another difference between the two percepts which cannot
be explained away and cannot be reconciled with the idea of a com-
pletely identical basis for the two. The movingnesses seen in both cases
may seem much alike, but they have utterly different sources. In real
motion, the movingness-blur is of physiological origin, and resides in the
retina. The overlapped photochemical images which produce it are chron-
ologically older than the foremost, newest image of the moving object.
But in the ^-phenomenon it is obvious that the generation of the mov-
ingness cannot possibly commence in the brain until after the retina has
been hit by the second light — otherwise, what would determine the direc-
tion the movingness was to take? In some way however, the impression
of motion reaches consciousness before the impression of the final posi-
tion of the movement — the second light — gets there. The phsysiological
sequence of events is: id) reception of the first light; (b) reception of
the second light; (c) instigation of the fiUing-in process, the percept of
movingness. But the perceptual sequence is: (a) light in initial position;
(b) movingness; (c) light in its final position.

Real and stroboscopic movements are thus deceptively similar subjec-
tively; but the only things they share in common objectively are their
dependence upon similar conditions of brightness and distance, and the
role played in each by the persistence time. This is probably not a coin-
cidence, for the close imitation of real movement by apparent movement
under the same spatial, temporal, and intensity-conditions presumably
has some biological value. What it is, we cannot say. The writer would
suggest — most gingerly! — that perhaps when a primitive, stupid verte-
brate saw a moving object pass behind an obstacle and emerge again, he
could not be trusted to know that it was all one object, and not two
different ones, unless he had an automatic means of maintaining the one-
ness of the object during the moment when it was hidden from him.
Whatever the incentive may have been for the evolution of the 'fiUing-in'
process in the ^-phenomenon, it is difficult to see what good its retention
has done us — unless one belongs to the growing number who regard the
movies as an absolute necessity.

Stroboscopic Vision in Animals — It is fairly certain that the lower
animals in general do have perception of stroboscopic apparent move-
ment. At least, it is well established experimentally for fishes and can be
inferred from such phenomena as the dog's interest in, and obvious
deception by, motion pictures, coupled with his complete indifference
toward still pictures. If apparent-movement perception exists for the

STROBOSCOPIC VISION IN ANIMALS 363

fishes, it probably exists all the way up to the dog and man. There
appears no positive reason why it should have been eliminated by any par-
ticular group, though it must be admitted that its usefulness is obscure.

The scanty experimental work indicates that stroboscopic movement
is seen by animals, as by man, as practically indistinguishable from real
movement of an equally luminous object over the same distance in the
same time. If further work is done along this line, and shows this rule
of 'identity' to hold firmly in case after case, we shall have a powerful
experimental tool for exploring animal capacity for real-movement per-
ception; for, as a matter of technical convenience, the ^-phenomenon
is more easily presented to an animal than is an equivalent real move-
ment. The apparatus is simple, and the control of such factors as accom-
panying noise is much easier. Variations are more easily introduced, for
it is far simpler to space two lights farther apart than to alter machinery
which moves one light back and forth.

A few years ago. Mile. Gaffron demonstrated stroboscopic vision in
two fishes, Phoxinus Icevis and Gasterosteus aculeatus, though with the
same technique she could find no evidence of it in various insects. The
dish containing the fish was surrounded by a cylinder capable of rotation
on a vertical axis and bearing vertical stripes on its inner surface. Rotated
slowly in either direction, the cylinder naturally evoked the optomotor
reaction — the fishes either swimming around with it or turning into a
radial position in which the eyes alone followed the movement. When
the cylinder was now illuminated intermittently, at different frequencies,
the fish responded to it as if it were motionless, or turning in its actual
direction, or turning in the opposite of its real direction, depending upon
the timing of the flashes relative to the positions of the stripes. Interest-
ingly enough, the apparent motionlessness, forward movement, and
apparent reversal of the cylinder were each seen by human observers
under the same conditions as by the fishes.

Almost simultaneously, von Schiller published his researches on the
stroboscopic vision of Phoxinus. He used a form of the (^-phenomenon
situation in which two white squares, set one above the other with a
certain separation, could be revealed at one end of the aquarium for vari-
ous periods and in succession at various time intervals. The fishes were
initially trained positive to an actual upward movement of a similar
white square, which was made a signal for food. Presented then with the
^-phenomenon, with the object, duration, and distance all identical with
the real movement to which they had been trained, the fishes responded

364 ADAPTATIONS TO SPACE AND MOTION

as if they were witnessing the real movement. The real and apparent
movements were completely interchangeable for them.

Moreover, Schiller was able to induce negative responses by lengthen-
ing or shortening the interval between the presentations of the two white
squares. When human observers were experiencing the successive or
simultaneous phases of the illusion, the fishes were negative. Within the
range of the optimal phase for humans, the fishes responded positively.
Schiller concluded that the three phases exist for Phoxinus and for man
under identical conditions. This would seem to imply that both species
have the same persistence time, at least under the adaptation-conditions
of the experiments.

Mile. Gaffron and Schiller both stress the fact that the fishes have no
cerebral cortex, and that therefore they (and man?) must 'see' apparent
movement with some lower visual center. Schiller beUeves further that
the mechanisms for real- and apparent-movement perception must be
one and the same, and suggests that in apparent movement we "see
with unstimulated parts of the retina." Since intermediate parts of the
retina need not be stimulated in a real movement in order to perceive
the movement, Schiller goes so far as to say that it is incorrect to call
stroboscopic movement an apparent movement — it is as real as any other,
physiologically. But, though the movingness of this phenomenon is per-
haps registered in man somewhere below the visual cortex, it is the blurred
train of after-images — assuredly registered in the cortex — which puts mov-
ingness into the percept of a real movement of our 'medium' category.*

The identity of persistence times in Phoxinus and man seems to be an
accident. In the Siamese fighting-fish, Betta splendens, Beniuc found a
much shorter period. He cleverly demonstrated both the biological
moment and the existence of complementary colors for this fish in a
single experiment. The fishes were trained positive to a gray disc and
negative to a slowly revolving disc whose six sectors were alternately of
two colors which are complementary for humans, yielding gray when
mixed by rapid rotation.

When the disc rotated at a speed at which its sectors gave the fish
130 impressions per second, the fish responded to it as if it were the
motionless gray disc. Beniuc found that at 90 impressions per second

*Pbtzl has described psychiatric cases in which the movingness of real movements was not
seen. A moving light was perceived as several lights in a series of positions — for all the
world like the appearance of a phi-phenomenon, in its successive phase, to a normal person.
It is impossible to say just what part of the normal equipment is lacking in such individuals.

THE PECTEN AND MOVEMENT-PERCEPTION

365

(far above human fusion frequency) the fish was still clearly perceiving
the rotation. At 100-120, the fishes reacted poorly, and were probably
experiencing flicker. 110 impressions per second was the lowest limit for
fusion. Beniuc translated this figure into a value of V55 second for the
duration of the biological moment of the Siamese fighting-fish.

Menner's Theory of the Pecten — The pecten of the bird eye (see
Figs. 80, 114; pp. 188, 308) has been one of the greatest puzzles in
comparative ophthalmology. Some years ago an authority counted over
thirty theories as to its function, which were sufficiently different to call
distinct interpretations. Other suggestions have been made since, but
none more intriguing than the very recent one offered by Erich Menner.
The pecten (Fig. 114, p. 308) is a simple cone in reptiles, where it
cannot possibly play a role in vision but is merely a nutritive organ, on
a par with the falciform processes, retinal vessels, and chorioid 'glands'

Fig. 127 — Overall tracings of the shadows cast by the pecten in each eye, in various species

of birds, in relation to their feeding habits and their consequent needs

with regard to movement-perception. After Menner.

a, Buteo buteo (a hawk, feeding largely on cursorial prey), b. Coal titmouse, Parus ater
(chiefly insectivorous), c, English sparrow, Passer domesticus (chiefly granivorous ) . d,
Domestic pigeon, Columba livia (granivorous). e. Long-eared owl, Asio otus (predaceous,
but largely dependent upon audition).

of Other vertebrate categories. In birds, however, it is an elaborately
pleated fin of pigmented and richly vascular tissue, reaching from the
retina nearly to the lens (Chapter 17). One can account for its great
increase of surface, over that of the reptilian organ, on the basis of the
bird's warm-bloodedness and elevated metabolism. But ulterior meanings
of this conspicuous organ have long been sought, the search stimulated
by the enormous variability of the pecten from species to species, and by
the hope of correlating these variations with something else in the visual
biology of birds. Briefly, the pecten is smallest, with the fewest pleats, in
nocturnal birds. It is larger in seminivorous forms, still larger and more
elaborate in insectivorous birds, and largest of all in the diurnal pred-
ators such as the hawks and eagles.

Menner placed numerous bird heads in a special perimeter and studied
the pecten with the ophthalmoscope from many angles. He found that

366 ADAPTATIONS TO SPACE AND MOTION

the pecten casts a shadow on the retina and that the tips of its pleats
extend this shadow, like the fingers of a hand, across the fundus and
the neighborhood of the area centraUs. Figure 127 shows sample over-all
shadows — composite sketches made with many directions of the ophthal-
moscope light, from birds representative of various categories.

Menner felt that the dactyloid shadows of the pleats might be a device
for enhancing the perceptibility of movements. To test this idea he
aimed a camera, focused for infinity, at some circling birds in the sky.
On the ground-glass screen, nothing could be seen. He now glued to
the inside of the glass a cardboard model of the pecten which would cast
finger-like shadows. With the camera pointed again at the wheeling
birds, their movements and courses were at once evident upon the screen.

The phenomenon was then explained in terms of some old statements
of Exner, who found that a movement was especially conspicuous when
the image swung back and forth across the blind spot — the head of the
optic nerve. The repeated 'on' and 'off' effects gave the movement
greater saliency in consciousness. Menner decided that the multiplicity
of pecten-pleat shadows must do the same thing, in a big way: each
shadow, if pronounced {i.e., in strong illumination) would create a tem-
porary blind spot or streak, over which the swinging image would have
on-and-off impacts on the retina and in consciousness. He pointed out
that the development of the pecten in different birds (y.s.) goes hand
in hand with their need, considering their feeding habits, of good visual
movement-perception.

It had long since been decided by others that the development of the
pecten in various birds is correlated with their ranges of accommodation,
though no one has demonstrated that the pecten plays any part in the
process of accommodation in birds or reptiles. Now of course good
accommodation, high visual acuity, and acute movement-discrimination
would all be expected to go together in birds anyway — all being lowest
in the owls, highest in the hawks, with the granivorous birds and the
bug-eaters fitting neatly in between. These correlations do exist; and so,
as far as Menner's theory is concerned, the relationship he points to
(between pecten and habits) would exist whether his theory has any
value or not. The different ecological types of birds do need different
movement-seeing abilities, but their visual acuities alone, and their
persistence times, are probably already related nicely to their needs in
this respect without taking the pecten into account at all.

It is not entirely certain that the pecten, which is always located

MULTIPLE OPTIC PAPILLA 367

ventrally along the course of the embryonic fissure (see p. 107) ever
casts a shadow on the fundus at all unless the bird looks up at the sky.
The shadow may not often be very useful in terms of Menner's hypoth-
esis; and, assuming that there usually is a shadow, it may not operate
entirely as Menner believes it to. Any moving object — the object itself,
not its motion — should be seen more clearly if seen intermittently. One
can often count the blades of a rotating electric fan by blinking the eyes
rapidly so that each glimpse is only momentary. This, in fact, is the
very essence of stroboscopy — everyone knows that it takes a fast camera
shutter to 'stop' fast motion.

If a moving object is seen only intermittently, its nature can be better
made out since each image of it on the retina is less blurred by dragged
after-images. But it does not seem as if the fingers of a pecten shadow
are numerous enough and sufficiently close together to afford a series of
snap-shots of a moving object, analogous to those obtained by Eadweard
Muybridge's row of cameras. And if they were, they would hinder vision
in general for the bird, which would hardly benefit from being made to
look at the world as if through a picket fence. But if there is anything
to Menner's theory, it may help to explain another peculiarity of ocular
structure : multiple optic papillae.

Multiple Optic Papillce — In a number of fishes (for example Amei-
urus, Misgurnus, Polyipnus, and Polypterus) , in various salamanders,
and in members of the deer family, the optic nerve on approaching the
eyeball divides into as many as a dozen or more separate rootlets, form-
ing an equal number of separate little blind spots with functional retinal
tissue around and between them. In the squirrels (pp. 179-80) we saw
a deformation of the blind spot which is intended to minimize the
scotoma effect, thus promoting overall visual acuity. The situation in
the Cervidas may have this same meaning. But the multiple blind spots,
which look as though they might have the same purpose of avoiding a
single huge scotoma, mostly occur in forms with abysmally low visual
acuity. Of the fishes listed above, Polyipnus is a deep-sea form, and none
of the others has much, visually, beyond brightness- and movement-per-
ception. Such animals have not needed the break-up of their blind spots
to enable them to see more sharply, for they are beyond any such help.
But if a turning on and off of the reception of a moving retinal image
helps the movement to break into their dull minds, the multiple papillae
may do for them what Menner thinks the pecten does for the birds.

Chapter U

ADAPTATIONS TO MEDIA AND SUBSTRATES

(A) Aquatic Vision

Definition — Before we consider the requirements and consequences of
seeing through water we need to decide what we mean by aquatic in this
connection. There is no doubt that all but a few jfishes are aquatic; but
one may read in one book that the seal is an aquatic mammal, and in
another that he is an amphibious vertebrate. We may have to be a little
arbitrary about our definition of 'aquatic', arriving at it by a process of
elimination, and justifying our arbitrariness only in a later section.

The Amphibia (amphi = hoth., 6/05 = life) were given their name be-
cause they spend part of their lives in water and part on land. The word
amphibian means a member of the Class Amphibia. It is sometimes used
as an adjective, but should be avoided in favor of amphibious. This word
is much older than the scientific term Amphibia, and does not really
connote the same thing at all. Amphibious animals are those which are
in and out of the water off and on as an everyday thing, and 'equally
at home' in both media. Very few members of the Amphibia behave at
all in this way. Most of the common frogs (family Ranidae) do. The
less familiar but much more numerous tree-frogs, toads, and land sala-
manders do not. Most amphibians, then, are not amphibious. Rather,
they are aquatic for a part of their life-cycles (as tadpoles) and terres-
trial for the remainder with only brief annual visits to water to breed.
Some salamanders and a few anurans (e.g., Pipa and Xenopus spp.,
Telmdtobius micro phthalmus) never leave the water — they are as aquatic
as any fish. A few anurans (e.g., Hyla zeteki) never enter ponds or
streams, their eggs developing in mere spoonfuls of water between the
leaves, or in the central core, of bromeliad plants; and these forms are
as terrestrial as a human — whose embryo, inside the amnion, also floats
in water. The salamanders Hydromantes italicus and Oedipus adspersus
are thoroughly terrestrial, and give birth to their young.

We shall consider as aquatic, then, those vertebrates which never leave
the water. These animals with strictly aquatic vision include nearly all
fishes, some amphibians, the sea-cows, and the whales. It so happens that

368

WATER AND THE PLAN OF THE EYE 369

few of these ever even put their heads out of water for more than a
moment, and are not then demonstrably trying to see through air.

These animals which fit our definition can be expected to have no
compromises in their eyes, and to have these organs wholly devoted to
seeing through water. But we do not know what to expect from the eye
of any amphibious vertebrate until we learn whether he uses his eyes
more in one medium or in the other, or equally in both. Many of the
adaptations discussed in this section naturally occur in some or in full
degree in the few amphibious fishes, as also in the amphibious species
which are to be found in every order of the classes of amphibians and
reptiles, and in many orders of both birds and mammals. Those losses
and new acquisitions involved in the restriction of vision to the aerial
medium are dealt with in the succeeding section of this chapter; and the
particularly stringent ocular requirements of any animal which attempts
'amphibious' vision are considered in the third section.
Effect of Water upon the Plan of the Eye — It must never be for-
gotten that the vertebrate eye originated in water. Only when this is
firmly in mind can we grasp the full meaning of some of the most fun-
damental features of ocular anatomy and physiology. When the verte-
brates finally took the eye on land with them, they had perforce to fill
it and surround it with simulations of its original medium of action,
salt water — even as the spiders, coming to the land, remained dependent
upon a bit of their old environment which they bottled up in their
gill chambers.

Most of the physical and chemical properties of water affect the eye
or its operation. Many of these properties are essentially simple exagger-
ations of those of air — the greater absorption of light, greater scattering,
greater pressure-changes with altitude or depth, greater friction and so
on. But the quantitative disparity between air and water, with respect
to a given property, is so very great that in its evolution the aquatic eye
responds qualitatively to factors whose air equivalents are negligible
to it and evoke no adaptive response at all.

Before the evolving eye produced any precise adjustments to the
purely optical properties of water, it had first to attain harmony with
properties which affect all animal organs and tissues exposed to that
medium, whether they are photosensory or not. The phenomenon which
unquestionably had a more profound effect than any other upon the
fundamental design of the vertebrate eye was osmosis, which therefore
receives first consideration in our discussion.

370 ADAPTATIONS TO MEDIA AND SUBSTRATES

When the two sides of a Hving membrane are bathed by liquids con-
taining differing amounts of dissolved substances, there is a net flow of
water through the membrane toward the side of the higher concentration.
The easy way for a living cell, or a whole organism, to maintain its
water content is to take advantage of this fact and expose its salty proto-
plasm to plain water, with a semi-permeable membrane intervening. A
freshwater organism therefore need not drink water, for plenty of it is
penetrating his surface continuously under the drive of osmosis. But in
getting his water in this way the animal is literally playing with explo-
sives. Unless controlled in some way (usually by excreting water about
as fast as it comes in) the pressure built up inside the cells by osmosis
will carry them past the desirable degree of turgidity, and will burst
them. The freshwater organism has this problem of osmosis-control more
urgently than the marine organism, for the disparity of concentrations
of dissolved substances within and outside the body is far greater. More-
over, the freshwater form must provide against the loss of essential salts
in the excreted water. We know, however, that the ancient seas were far
less salty. While it is often said that the vertebrate blood was originally
entrapped sea-water (the concentrations of salts in human blood there-
fore supposedly portraying the chemical pattern of the Devonian ocean)
we may be sure that the protoplasms of marine animals of the remote past
had higher osmotic pressures than that of the water outside — it would
have been disastrous for protoplasm to have become otherwise. There is
considerable evidence that the first vertebrates arose in fresh water, and
we can be quite sure that the land animals evolved from freshwater fishes.
Even at the present time it is the marine fish, not the freshwater one,
which exhibits special devices in connection with the control of water-
balance.

The rigidity of the vertebrate eye, which makes it a good optical
instrument despite its constitution from soft and flexible tissues, is due
to a bit of hydraulic trickery. The eye owes its firmness to the fact that it
has a flexible but inelastic capsule which is kept distended by fluid pres-
sure. The same principle makes a hollow tennis ball just as firm as a
solid handball, and would allow us, if it were necessary, to put mobile
objects inside the tennis ball — a point which will seem important in a
moment.

The primeval source of this distensive intra-ocular pressure was osmosis.
Some excellent invertebrate eyes (as in some cephalopod molluscs) have
employed this force in the same way. In others, such as the compound

ORIGIN OF INTRAOCULAR FLUIDS 371

eyes first evolved by the crustaceans, the trick was never hit upon. Such
eyes being soUd, there is no possibility of rapid, gross, internal move-
ments for accommodation, regulation of incoming light, and so forth.
The vertebrate eye at the very outset received a tremendous boost
toward its eventual superiority, when it luckily developed a vesicular
plan of organization.

Origin of Intra-Ocular Fluids — In the eyes of the higher vertebrates,
we can put our finger upon the immediate source of the internal fluid.
It is certainly the ciliary epithelium, covering the ciliary folds and proc-
esses (Fig. 3, p. 7). But in the lowest vertebrates we see no such secretory
structures, and a fertile field awaits the investigator of the sources of
their aqueous humors.

Comparative physiology indicates that until there was need of an
intra-ocular secretory epithelium, there was no ciliary body. And, until
there was a ciliary body there could be no ligamentary anchorage of the
lens, and no lens-squeezing methods of accommodation. We do not
know for certain that the modern fish eye gets its water by osmosis
through the cornea; but in the absence of any experimental work on this
whole question, the assumption of such a process would explain much
of the anatomical simplicity of the piscine anterior segment. The absence,
from fish eyes, of those structures which terrestrial eyes have had to
produce or have found it possible to produce, in consequence of their
removal from water, is not adaptation to environment — unless one
extends the term to include refraining from producing anything which
is not needed. But these simplicities of the fish eye and complexities of
the terrestrial eye are certainly related to environmental differences,
rather than primarily to taxonomic ones.

All lampreys begin their lives in fresh water, and thus have the oppor-
tunity to fill their eyeballs by osmosis via the cornea, maintaining the
desired intra-ocular pressure by controlled drainage through the ocular
blood vessels. The several large, parasitic species which make their way
to the sea must surrender any such ability unless they are able to raise
the osmotic pressure of their intra-ocular fluids by excreting salts, glu-
cose, or other substances into them. Failing this, they must somehow be
able to secrete more fluid inside the eye from some of its tissues, even
though we can see no special anatomical provision for such secretion.
Moreover, since the marine lampreys are anadromous, they must shut
off these compensatory intra-ocular secretions when they return to fresh
water at the end of their lives to breed.

372 ADAPTATIONS TO MEDIA AND SUBSTRATES

It would seem that there must also be a difference in the source of
the water of the humors in fresh- and salt-water teleosts. The former are
known to admit water readily everywhere through the skin, and to pro-
duce large volumes of urine in consequence. The marine teleosts, de-
prived of this use of osmosis, must fight for their internal water. They
swallow sea-water and absorb it from within, excreting the excess salts
by means of special cells in the gills.

No consistent differences have been reported between the eyes of
freshwater and marine teleosts. If in the former the intra-ocular fluid
and its pressure are recruited by osmosis through the cornea, it becomes
a mystery where these come from in the marine form. If the latter gives
off aqueous from the iris, falciform process, or hyaloid vessels, does this
occur — and if not, what prevents it — in the freshwater eye? And, there
are both anadromous (e.g., the Pacific salmon) and catadromous (e.g.,
the common eel) teleosts, whose eyes appear the same as regards possible
secretory structures whether they are in fresh water or salt.

The elasmobranchs are mostly strictly marine though some, like the
sawfish (Pristis) may enter perfectly fresh water; and several species are
landlocked. All are known to maintain a high level of urea (2%) in
their blood to give it a slightly higher osmotic pressure than the sea-water,
so that they have as easy a time to maintain their general water balance
as does the freshwater teleost; and like the latter they do not need to
drink. They form little urine except when in fresh water, when they pro-
duce 50-100 times as much. In Squalus, at least, the intra-ocular fluids
have been found to have a still higher osmotic pressure than that of the
blood. It is therefore easy to believe that the intra-ocular water can come
in through the cornea and that the intra-ocular pressure can be automat-
ically regulated by controlled osmotic pressure; but it is a disturbing fact
that the elasmobranchs are the only fishes which have ciliary folds (Fig,
104, p. 259), This makes it look, at first glance, as if they secreted their
aqueous just as a land animal must. The ciliary folds are low and no
more heavily vascularized than epithelial folds generally are, however,
and moreover are blanketed (except where they continue, even lower,
onto the iris) by the thick peripheral rim of the gelatinous 'zonule'. They
do not appear to be advantageously organized for secretory purposes. Is
their function purely mechanical, to increase the surface of attachment
of the zonule? Franz believes so, since he found them best developed in
the species with the most powerful lens-muscles. Are they even absorp-
tive, the cornea being unable to control the amount of incoming water,

EFFECTS OF WATER UPON LIGHT 373

and letting through an excess as compared with that of a freshwater tele-
ost? No experiments have been made to test this interesting possibility.

Effects of Water upon Light — Some other properties of water, salt
or fresh, which affect aquatic vision per se regardless of the interspecific
variation of fishes in their general make-up, are those which alter the
amount and kind of light passing into and through it. To a vastly greater
extent than in air, horizontal distances and vertical distances through
water are not optically equivalent. As sunlight penetrates downward into
water, it undergoes extinction, which is a blanket term embracing both
absorption and scattering. Off Plymouth, England, 90% of white light
was found to be extinguished at eight or nine meters, 99% at 35 meters.
These effects vary from one body of fresh water, or part of the sea, to
another and there is no close agreement between investigators as to what
is normal or average. Roughly however, a depth of 535 meters in the
clearest waters is characterized by utter darkness as far as human vision is
concerned. Beebe found only a 'bluish glow' at 435 meters off Nonsuch
Island. Some seas are completely dark at 200 meters, dirty harbors in a
few meters. Even the clear Bermudian seas seemed to Beebe the 'blackest
spot on earth' at a depth of half-a-mile.

The various wavelengths of light do not all reach to the same depth.
The ultra-violet is almost all eliminated in a few millimeters of water,
though traces reach to greater depths than any other wavelengths —
enough, at 1000 meters, to affect a photographic plate, though only after
80 minutes exposure! The infra-red (heat) rays are cut out in a few cent-
imeters, or a meter or so. As the light descends, the ends of the spectrum
are pared off, the long-wave end more rapidly (90% of the red is gone
at five meters) , until a band is left whose wavelengths continue to pene-
trate about equally well. The limits of this band, as determined by a
photographic technique, are from A,510m[X to X540m[J,. Beebe, in the
bathysphere, reported that at 250 meters all that was left of the spectrum
was a narrow band centering at X520m[l. This visual observation checks
well enough with the results obtained by lowering remote-control cameras
to various depths. Not that there is much of this light — 90% of the
green part of sunlight is already extinguished at thirteen meters.

It is more than a coincidence that these best-penetrating wavelengths
should be identical with those to which fish rhodopsins are most sensitive.
The rhodopsins of land animals have their absorption maxima averaging
at around A,500m(J, (that of the ox, for example, is X495m^ — of man,
about A,500m|l) ; but it must be remembered that the first rhodopsin was

374 ADAPTATIONS TO MEDIA AND SUBSTRATES

invented by pro-fishes, and partly for the purpose of allowing them to go
down from the surface to the less brightly lighted depths. A group of
English workers recently found that the absorption maxima of a num-
ber of marine fish rhodopsins range from A,505m[X to A,545m[l. They
hoped to find a relation between the particular maximum of a given
species and the depth preferred by that species. This was not established;
but the investigators failed to take the broader viewpoint, from which
one can see that since the A,510-540m|X band penetrates deepest, it
will be most conspicuous in the spectrum at any lesser depth. And since
the sun's rays within this range have equal facility of penetration through
water, a rhodopsin would be maximally efficient with its absorption peak
located anywhere in this band.

There may be a close adjustment of a particular fish to a particular
quality of light available at his preferred depth — it may be that the in-
vestigators mentioned were simply unable to obtain sufficiently accurate
information as to just what depth a given species does prefer. More prob-
ably however there is a weight of other factors which usually make it im-
possible for a fish to be at all precise in this matter. A sandy-bottom
species like a flounder, for instance, has to be content with bottoms which
vary considerably in distance from the surface. Even more upsetting are
the barrier-effect of the thermocline and the seasonal turnover of lakes,
for a fish which responds to critical temperatures may swim at one depth
for a part of the year and at a very different depth, or at no particular
depth, for another period. Still other fishes may be free of any control by
the thermocline and still show no close restrictions as to depth. The wall-
eyed pike, for example, remains in deep water by day and comes into the
shallows to feed at night. Many marine fishes also show such rhythms.
Astronesthes, for example, lives in the gloom at 200 meters by day and
follows the twilight upward to spend the night at the surface. Such fishes
are responding to a particular quantity of light regardless of the time of
day, or the depth, at which they find it, and not to a quality of light
which is characteristic of a particular depth when the sun is high.

Since we are thus led to expect only a very general correspondence
between differential sensitivity and depth of swimming, the A,505-545m[X
range of rhodopsin maxima seems close enough to the A,510-540m|l band
of best-penetrating wavelengths to give us the right to say that the very
color of rhodopsin itself, like the ruddy color of some photosynthetic pig-
ments of the deepest-living seaweeds (Rhodophyceas) is an adaptation to
water. That same red color, in human rhodopsin, is still another heritage

EFFECTS OF WATER UPON LIGHT 375

from our immensely remote aquatic ancestors. If rhodopsin had been first
invented on land, it might very well have been purple, not red.

In some freshwater and anadromous fishes it has recently been found
that the absorption maximum is roughly intermediate between those of
marine fishes and land animals, the value being ^522 ± 2m|i,. The investi-
gator (Wald) has called the photosensitive substance involved 'porphy-
ropsin'; but there is little excuse for the new word. Rhoddpsins have been
re-invented so many times that if we coined a new name for each one
that we can distinguish chemically or spectroscopically, the nomenclature
would soon be hopelessly confused. There is even good reason to think
that in marine fishes there are two rhodopsins simultaneously present,
the effective absorption maximum of the rods being dependent upon the
relative amounts of the two.

An important effect of depth upon light-quality is happily significant
for every fish. This is the rapid extinction of ultra-violet. In this part of
the spectrum there is one band of wavelengths, from 295m[i to 305m[l,
which is particularly harmful — positively lethal, in fact — to living tissues.
This is consequently known as the 'abiotic' range. No aquatic species need
concern itself with protection from abiotic light; for even if the water
were chemically pure, a few millimeters would absorb it all. The dis-
solved and suspended matter of natural water disposes of it even more
promptly, by fluorescing it into harmless visible light. Land vertebrates,
diurnal ones at any rate, have had to evolve a capacity for fluorescence
by their lenses. Aquatic forms frequently show no such capacity, for they
do not need it. Stickleback and toad lenses are very transparent to ultra-
violet, frog and carp lenses less so.

More important than the qualitative effects of water upon light are its
quantitative ones. Even if extinction with depth were not selective, it
would still affect aquatic vision profoundly — as is emphasized by the vis-
ual problems of the deep-sea fish, shortly to be considered. Even close to
the surface, vision in the horizontal direction is greatly dimmed. To put
the matter crudely, we cannot see the side of a light-beam — only its end,
and for light to enter the eye it must be sent or reflected directly toward
the organ. Under water, there are not nearly as many reflecting objects
in the plane of the eye of a fish — particularly in the open sea — as there
would be on land. Such light as is aimed at the eye is weaker because
there are few hard and smooth, hence brightly reflective, surfaces; and
this weak light is further weakened through scattering by suspended
matter. All in all, if a fish or whale can distinguish objects fifty feet

376 ADAPTATIONS TO MEDIA AND SUBSTRATES

away at his own level, it is a red-letter day for him. With increasing
depth, or increased turbidity, this distance is still further reduced since
the absolute amount of light reflected into the eye of the animal depends
upon the relative amount of sunlight reaching that depth.

Under water, vision is handicapped while other senses are actually
promoted. It is not surprising that the fishes are better able to get along,
if blinded, than any other vertebrates. They use their eyes when they can,
but most fish can find enough to eat without seeing the food. Many fishes
are deprived of vision in winter, when the ice above them is blanketed
with snow, and some arctic species live out their whole existence under

Fig. 128 — Fish from above, showing visual angles in the horizontal plane.

This particular fish does not have complete periscopy — with a less bulky body the posterior
blind angle would diminish; but the anterior binocular field might then also be reduced.

b- binocular field; m, m- monocular fields; u, u- residual, uniocular fields; x, x- anterior

and posterior blind areas.

such conditions. No wonder, then, that so many fishes have been able
to establish themselves and survive in lightless caves.

The optical density of water has interesting consequences upon aquatic
vision, particularly upward through the surface and into the air. Re-
peated allusion has already been made to the fact that the corneal tissue
has about the same refractive index as water, so that the cornea is in
effect optically absent under water, and the first bending of incoming
light-rays takes place at the surface of the lens. This requires the lens to
bulge far through the pupil if that aperture is not to limit greatly the
visual field (Fig. 105b, p. 261); and the lens must project from the sur-

LOOKING THROUGH THE SURFACE 377

face of the body itself if periscopy — 180° vision for either eye, 360°
vision for the two together — is to be attained in a fish whose eyes are
back to back (Fig. 128). To many a swift form — the tuna, for example —
streamlining is more important than periscopy, and the eye is not allowed
to protrude. The broad cornea of a fish eye is not at all related to light-
gathering power as it would be in a land animal — the relative size of the
pupil, by itself, determines the brilliancy of the retinal illumination (see
p. 211).

The importance of periscopy to a fish is not only seen ecologically, in
his increased awareness of near-by prey and increased difficulty of
approach by enemies, but is also seen anatomically in his lack of a neck.
Despite his buoyancy and rotability on his vertical axis, a fish would need
a neck almost as badly as a land animal, were it not for his full visual
field. Periscopy has not been important to whales, because vision itself is
unimportant to them; but the seals have retained it by keeping the neck
flexible — which the whales and sea-cows have not done.

Looking Through the Surface — When the surface is almost literally
as still as glass, an underwater animal can look up through it, but with
such peculiar consequences that they may account for the bewildered
expression of the average fish! A light ray passing through a rarer
medium and striking a denser one will enter the latter from any angle of
incidence; but for rays passing from denser media into rarer ones, there
is a 'critical angle' of incidence at which they are bent just enough to
skim the boundary surface. At greater angles, they are totally reflected
and cannot escape into the rarer medium at all. With light, there obtains
just the inverse of the situation when a gun is fired at a submerged sub-
marine— if the boat is too far away and the angle of fire too flat, the
shell cannot enter the water, and reflects, ;'. e. ricochets, harmlessly from
the surface.

The consequence of this is that if a fish looks slantingly upward at the
surface, he cannot see through it, but instead sees mirrored upon it
objects which are on the bottom at a distance (Fig. 129). If he looks more
directly upward, he sees into the air. In effect, there is a circular window
in the surface through which he can look (Fig. 129a). This window
enlarges if he sinks, shrinks if he rises, but always subtends an angle of
97.6° (in fresh water) at his eyes. If the bottom is distant, the surface
outside the window is silvery with the reflection of the light scattered in
the water, and this light of course always washes over and dilutes the

378

ADAPTATIONS TO MEDIA AND SUBSTRATES

image of the bottom, even when the latter is close enough to the surface
to be seen reflected from it.

Through his surface window the fish sees everything from zenith to
horizon in all directions. This hemispherical aerial field is not narrowed

Fig. 129 — Visual field of a fish in the upward direction.

a, the water surface and the aerial window as seen from beneath, b, explanation of the
window: rays striking the surface at an angle within the window are refracted to the eyes
of the fish, but rays striking outside the window from beneath are totally reflected. Within
an angle of 97.6° the fish sees out into an aerial hemisphere; but outside of this angle he
sees objects on the bottom, reflected in a silvery surface. The surface must of course be
completely calm.

or widened according to the size of the window and the depth of the fish.
It always contains everything above the plane tangent to the water sur-
face at the rim of the window, but the distortion and the brightness of
objects within it do vary. The objects seen proportionately largest are

STREAMLINING OF THE EYEBALL 379

those directly overhead. If an object should swing down a semicircle
from the zenith toward the horizon, along a meridian of the aerial hem-
isphere, it would get shorter and shorter in its meridional length and in
its width measured parallel to the surface. Thus even though its linear
distance from the fish were constant, its apparent size would become
smaller, the closer it approached the horizon. It would be seen more and
more dimly, too, for light rays which make small angles with the water
are largely reflected, and but little of such light is refracted down
through the surface to enter the eye of a fish.

The entire circumference of the 'horizon', which a swimming man
could see by treading water and rotating 360° on his axis, is, for the fish,
contracted to the few inches or feet of circumference of his surface win-
dow. It follows that a man standing on the bank of a pool is seen as a
tiny doll by a fish which is a few yards away and only a few inches below
the surface. Our tendency is to suppose that the fish will see us more
poorly still, just as we see him less well, if he drops deeper in the water;
but since dropping lower enlarges his window, it magnifies objects on the
shore — magnifies them, that is, as compared with their apparent size
when the window is smaller. To see the fisherman optimally, then, the
fish must seek a depth from which the improvement of visibility through
enlargement is not cancelled by the loss of light through the greater dis-
tance of water through which the rays must travel to his eyes. The poor
fish is thus fated never to see us as we are — even through the flat glass
side of an aquarium tank.

Streamlining of the Eyeball — Except in placid, slow-swimming
species, the fish eye must ordinarily bear some structural adaptations to
its propulsion through the water. The considerable resistance of the
medium has two effects upon the eye of a fast-moving fish: friction, tend-
ing to scour and erode the corneal epithelium; and asymmetrical pressure.
To combat these effects the eye, like the body as a whole, must be stream-
lined. The ocular streamlining is of some importance in reducing general
bodily water-resistance; for the contribution of the eye, though it may
bulge only a bit from the head, is not negligible. The streamlining of
the eye affects the eye itself, and helps substantially to maintain the
optical status quo: the moving cornea receives added pressure on its
advancing nasal border, and at the caudad border of the exposed part of
the globe a region of lowered pressure exists as on the upper surface of
an airplane wing. These differential pressures would lead to a distortion

380 ADAPTATIONS TO MEDIA AND SUBSTRATES

of the eyeball, and to a disturbance of its optical performance, if they
were not somehow minimized.

The reduction of friction and of the asymmetry of pressure is partly
effected by the ellipsoidality of the eyeball. The visual axis of the fish
eyeball, as we have seen, is almost always its shortest diameter. Its hori-
zontal, cephalo-caudal diameter is commonly its greatest dimension, and
may exceed the vertical diameter by fifty per cent or more (Fig. 104,
p. 259) . Thus the pelagic fish eye, partly for the sake of streamlining and
partly for the sake of a wide horizontal visual angle — which swift fishes
of course desire — is not a ball, but is rather an 'ellipsoid of revolution'. It
presents to the water a portion which, as to curvature, is shaped like the

Fig. 130— Scleral ossicles in fishes. After Edinger.

a, an arthrodire, Dinichthys gouldii, exemplifying the four-part ring characteristic of many
ancient fishes, x J4 b, pike, Esox lucius; scleral cartilage and the two ossicles character-
istic of modern teleosts. x 1. c, tuna, Thunnus thynnus, showing return to complete ring
(which, however, involves but two ossicles), x Vi.

bowl of a teaspoon; and, of course, the part of the eyeball which shows
through the lid-opening can still be, and often is, quite circular in out-
line— just as we can easily cut a circular piece out of a teaspoon. Past
the teaspoon-surface, which is often a part of the head-surface itself, the
water may stream with the least possible distortive action. The cornea
may be rendered violently astigmatic by its dual curvature (see Fig. 13,
p. 28) , but since its surface is under water, no optical harm is done. The
spherical lens, alone, is forming the image on the retina.

In lampreys the ellipsoidality or horizontal elongation of the eyeball
is very slight, but the eye is smoothly covered by the primary spectacle
anyway (see section D). Ellipsoidality is very marked in many elasmo-
branchs, which are often swift swimmers as their predatory habits natur-

'ADIPOSE LIDS' 381

ally require them to be. The cornea is not flat as in teleosts, since the
elasmobranch lens must have room to move forward in accomjnodation;
and the outline of the cornea is often involved in the ellipticity, being
then much broader than it is tall. Practically never — Lamna is an excep-
tion— is the vertical diameter of the cornea at all greater than the
horizontal. The cornea is thin centrally, and markedly thickened toward
its rim (Fig. 104), a construction which makes of it a more sturdy dome
than it would be if it were uniformly thick, and also leaves more room
for the lens to increase its distance from the retina. Among the chon-
drosteans and holosteans, the shark-like sturgec^ns and the gars (which
make swift dashes after their prey) have ellipsoidal eyeballs. Not so the
slow-swimming Amia.

In the teleosts a pronounced bulbar ellipsoidality is common, and the
cornea is often more or less oblong horizontally as well. Characteristically,
the piscine sclera consists largely of a cartilaginous cup, which is often
calcified (and, in Tetragonopterus, is entirely bony). In many teleosts,
additional support for the anterior part of the sclera is afforded by a
pair of osseous demilunes, disposed nasally and temporally around the
cornea (Fig. 130b), and sometimes fused above and below into a con-
tinuous ring. These demilunar ossicles are embedded in the connective
tissue of the sclera, and are best developed in the swiftest swimmers.
They are heaviest of all in the tuna (Thunnus) and the swordfish
(Xiphias), where they form a complete, deep 'napkin-ring' enclosing
nearly the whole of the eyeball (Fig. 130c). These ossicles have nothing
to do with the imbricated scleral ossicles of the Sauropsida (see p. 271),
which are homologous with the circumorbital bones of fishes. The demi-
lunes of modern teleosts probably represent the anterior and posterior
members of a quartet of ossicles which, in some of the oldest of fossil
fishes, formed a complete circumcorneal ring (Fig. 130a).

* Adipose Lids'— In addition to the streamlining effect of an ellipsoidal
cornea, supported by scleral ossicles, many swift teleosts possess so-called
adipose lids, whose effect is to cover the circumocular sulcus and thus
eliminate distortive eddies in the slipstream alongside the eyes (Figs.
131a and 132).

Considering their usual orientation, these lids are better called vertical
lids, for they are rarely truly adipose. Mugil cephalus forms an exception
— here, the lids are usually puffy, and may contain so much lipid sub-
stance that they turn yellow and opaque in preserved specimens. Ordin-
arily the vertical lids are very thin, and are perfectly transparent where

382

ADAPTATIONS TO MEDIA AND SUBSTRATES

they overlap the cornea. They consist of basophilic mucous, muco-areolar,
or sometimes fibrous or cartiloid connective tissue. In some forms, as
Scomber, they are said to become thickened and charged with fat during
the breeding season. In some species (salmonoids, particularly) they have
been described as anchored to orbital bones by special ligaments, or to be
movable by special muscles; but these points are in dispute.

In various pelagic teleosts, the vertical lids present themselves in essen-
tially three conditions. Typically, they consist of a pair of ingrowths
(minus an epidermis) of the skin which, in fishes generally, forms the
outer lip of the circumocular sulcus (Fig. 151b, w; p. 451) — the line of

Fig. 131 — Permanent lid-complexes in fishes.

a, head of a teleost, Scomber scrombrus, showing vertical ('adipose') lids in surface view

and in seaion. After Hein. b, left eye of a requin shark, Galeorhinus galeus. After Franz.

i- iris; //- lower lid; n- 'nictitating membrane'; s- sclera; ul- upper lid.

junction between the conjunctiva and the surface skin of the head. More
often than not, the anterior fold smoothly joins the posterior one above
the eye, but overlaps the posterior fold inferiorly (Fig. 132b, c, d, f).
A series of species could be selected in which, by imperceptible steps,
this situation would intergrade with one in which the cornea is sur-
rounded and overlapped by a practically circular, continuous fold, of
about the same width in all meridians (Fig. 132g). Various conditions in
this series may occur in the same genus, as in Mugil, Caranx, Scomber,
and others. The anterior and posterior lids may be equally developed, or
— much more commonly — the posterior may be the wider of the two.
Very rarely {e.g., in Mugil bleekcrii) the anterior is the broader. The

■ADIPOSE LIDS'

383

aperture between well-developed lids is a narrow vertical ellipse (Fig.
13 2d), but tends toward a large circle as the lids are reduced in extent.
Where the lids are narrow, they are usually continuous inferiorly as well
as superiorly, instead of being overlapped (Fig. 132e, g). There are in-
stances in which a given genus has prominent vertical lids, while a related
one with closely similar habits is without them, perhaps owing to total
disappearance. Tarpon for example has no lids, whereas the ten-pound-
ers (Elops) have them well developed.

Lids of the types just described are especially characteristic of the
herrings and their allies, constituting the 'clupeoids', among the soft-
rayed teleosts (Malacopterygii) . They have been independently evolved

w

A
N
T

L

R

'^v/>'"~V,

1

1©^I

0

"-----.--^/

R

Fig. 132 — 'Adipose' lids in various teleost fishes (drawn from preserved specimens).

a, Salmo gairdnerii irideus. b, Clupea harengus. c, Nematalosa nasus. d, Pomolobus
chrysochloris. e, Hiodon tergisus. f, Rastrelliger loo. g, Mugil cephalus.

/- fold or ridge in head skin; /n- 'false nirtitating membrane'; Mimbus corneae; m- margin of
drcumocular sulcus; o- wall of orbit; p- pupil; s- extremity of recess under m.

also by equally swift, pelagic members of the more advanced spiny-rayed
division ( Acanthopterygii) . The correspondence between Pomolobus
(Fig. 132d), a clupeoid, and Rastrelliger (Fig. 132f), a scombroid, is
quite perfect. Mugil cephalus, another acanthopterygian (Fig. 132g),
has its counterpart in the clupeoids /I m/)/?/Won and HjoJon (Fig. 132e).
Among both malacopterygians and acanthopterygians there are families
in which the aperture between the vertical lids has been quite obliterated,
so that there is an unbroken covering over the eye. Though this is of
course also a streamlining adaptation, and probably an even better one
than the separate, apertured lids, it is discussed later in connection with
the other types of 'spectacles' to which it is morphologically related.

384 ADAPTATIONS TO MEDIA AND SUBSTRATES

The salmonoids (salmons, trouts, whitefishes) present a condition
which differs considerably from both the two-iids-overlapped and contin-
uous-circular-fold extremes, and from any situation intermediate between
them. The salmonoid complex (Fig. 132a) consists of a narrow, crescentic
posterior lid running around two-thirds of the circumference of the eye
(and comparable with the posterior lid of a herring or a mackerel)
together with a broad, roughly triangular, anterior fold. The latter is
depressed below the surface of the head, for it is developed not from the
extreme margin of the circumocular sulcus, but as a separate conjunctival
fold arising from beneath that margin, on the anterior side of the mem-
branous orbit.

It is hard to say whether this arrangement has been derived from one
like that of the clupeoids, or is quite independent. Ecologically, it prob-
ably has a special significance. The eye is not actually as well stream-
lined as it would be if the anterior sulcal margin were to recede smoothly
into the head surface, thereby creating something more like the arrange-
ment in Hiodon. In the salmonoids, the bony orbit is incomplete anteri-
orly, and it may well be that they have taken the opportunity to draw
the anterior sulcal margin well forward, primarily to permit of more
straightforward vision and a wider binocular visual field during the pur-
suit of prey. The broad, stiff, anterior lid-fold of the salmonoids, which
has been called a 'false nictitating membrane' (Fig. 132a, fn), can thus
be thought of as having been left behind by the forward-migrating sulcal
margin (to prevent the opening up of a gap between the latter and the
cornea), rather than as having grown actively, posteriorly, toward the
center of the cornea as the anterior lids of the clupeoids and scombroids
have certainly done.

Bottom Fishes — A host of coastal fishes, both elasmobranchs and tele-
osts, have chosen to live on the bottom. By thus putting their backs
against a wall and living at the center of a hemisphere of space rather
than a sphere, they have halved the job of watching out for enemies and
prey. At the same time they are close as can be to a retreat or a cam-
ouflage— in crevices or burrows, or in the sand or mud with which they
can cover themselves. Living as they do in such intimate contact with
their chief food supply, the other members of the 'benthos' or bottom
fauna, many crevice- and mud-dwelling fishes have found vision of little
use, and have allowed their eyes to become small or degenerate — or even
to dwindle to tiny, blind remnants under an opaque skin (Fig. 133b,
p. 387).

BOTTOM FISHES 385

Other fishes have become adapted to live on, rather than in, the sub-
strate, most of these being dependent for concealment upon their incon-
spicuous shapes and colorations. The bottom elasmobranchs — the skates
and rays, the sawfish (Pristis) , the guitar-fish (Rhinobatos) , and the ray-
like shark Squatina — have a depressed form. A consequence of their dor-
soventral flattening has been an equal rotation of their two eyes so that
they look more or less upward — in Squatina, for example, the visual lines
slant upward at 45° angles. A number of teleosts have evolved the
depressed shape also, the angler-fish Lophius for example, and to a less
degree the stargazers (Uranoscopidae) ; but most flat-lying teleosts are
among the more than 500 species of the flatfish group :

In the flatfishes, the laterally-compressed animal has simply lain down
on its side (right or left, according to species) during its individual
development. The new under surface remains unpigmented and loses its
eye, by migration over the top of the head (or even through it) , to the
new upper or eyed side. In the more specialized flatfishes the mouth tries
its best to twist too, but not very successfully, so that it works largely
crosswise. The begirmings of the flatfish habit can be seen in some sea-
perches which habitually rest on their sides, the families Serranidae and
Labridae particularly. In one primitive tropical flounder (Psettodes
erumei) , the eye from the future blind side stops at the crest of the head,
never moving completely over onto the eyed side to join its non-migra-
tory fellow. Unlike other flounders, individual Psettodes may end up
lying on either the right side or the left — that is, either eye may be elected
to migrate. The dorsal fin commences behind the head in this species,
whereas in a perfected flatfish it waits until the migration of the eye has
taken place, and then grows forward — cutting off the eye's retreat, so
to say.

A topside position and approximation of the eyes brings with it an
advantage and a disadvantage, to either or both of which various fishes
have responded adaptively. The advantage is the opportunity to secure
an exceptionally broad binocular visual field, especially in an upward
direction, with a consequent improvement of space-perception. The dis-
advantage is that the eyes are subjected to dazzlement by the vertically
incident sunlight.

Some upward-looking bottom fishes have met the problem of dazzle-
ment by placing the eyes so that they can look horizontally, permanently.
The dorsal binocular field may then be largely sacrificed, of course, as
in Manta. Others, such as Lophius, are able to swing the eye downward

386 ADAPTATIONS TO MEDIA AND SUBSTRATES

until it aims horizontally, there being a special provision for this in the
form of a temporary lower lid. Still others have kept the eyes aimed more
nearly upward and have given them protection, from over-stimulation,
by means of expansible pupillary opercula.

Such an operculum is most nearly a group-character in the batoids
(i e., rays in the broad sense) .These elasmobranchs (but not Squatina)
lack the eyelids (Fig. 131b, p. 382) which characterize the bottom-loving
sharks (Galeorhinidce) , but they can nevertheless retract and 'close' their
eyes at times to shield them from strong light (p. 452). The eyes are
relatively small, as they are in all upward-lookers, which have not the
need for a large pupil that a lateral-eyed fish has. A ray's eyes are little
more than half the size of those of a shark of equal size. The pupillary
operculum ordinarily has a smooth margin (e.g., Torpedo, Trygon,
Myliobatis) , but in Raja it is serrated so that, on full expansion, it re-
duces the pupil to a crescentic series of stenopaic apertures (Fig. 65b,
p. 158). The operculum of Torpedo is small, but it can cut the slender,
horizontally oblong pupil quite in two. In the mantas or devil-fishes
(Mobulidae) and eagle-rays (Myliobatidae) , the eyes aim not upward but
laterally, due to the presence between them of a pronounced ridge of
head material. The mantas lack a pupillary operculum, though one is
present in Myliobatis.

A mutual exclusiveness of pupillary opercula and turreted orbits is also
suggested by the situation in teleosts. The operculum varies from small
(in the star-gazer, Uranoscopus scaber, where it is dentate — see Fig.
65d) to large (flounders), and is remarkably developed in the armored
catfish Plecostomus (Fig. 65e, f, g). The bulk of the flounders are in-
cluded in the families Bothidae (left-handed) and Pleuronectidae (right-
handed flounders) . In the bothids, the eyes tend to lie fairly flat in the
head, and an operculum (Fig. 65c) is the rule; but the eyes of pleuro-
nectids, by and large, lack opercula and can be elevated hydraulically, and
swivelled about in the horizontal plane by a special slip of the superior
oblique muscle. Some pleuronectids, however (e.g., Platichthys flesus),
do have opercula. The ocular turrets of flatfishes make it possible for
them to see even while the body is sifted over with sand for concealment.
A lateral aim of the eyes obviates any handicapping of the horizontal
vision of the animal when it rises from the bottom to become pelagic
for the nonce, as do the mantas, eagle-rays, and many flatfishes. The
binocular vision, now forward, now upward, of the turret-eyed flounders
gives these fishes what has been called an 'intelligent' look.

CAVE FISHES

387

While the eyes of most good-eyed bottom fishes look perpetually up-
ward, those of one genus, Corydoras, periodically look sharply down-
ward. These are tiny South American armored catfishes which are popu-
lar as scavengers in home aquaria, and they are commonly believed to be
'the only fish that wink'. Since there are no lids, there is no true wink —
the eyeball simply rolls downward until the pupil is largely or wholly
concealed; and the gray superior conjunctiva, which is thus exposed, does
give the appearance, from above, of an upper lid going into action. The
utility of this phenomenon is not apparent. It might be suspected that
the fish has an upwardly-aimed fovea, and has to turn the eye down to
use the fovea for occasional horizontal vision; but serial sections of a
Corydoras eyeball have revealed no such feature.

Fig. 133 — Microscopic, degenerate eyes of blind fishes. After Franz.

a, a hagfish, Myxine glutinosa (internal parasite), b, a goby, Trypauchen wakt (littoral,
crevice-dwelling), c, an amblyopsid, Troglichthys rosce (cave-dwelling).

Cave Fishes — The cave fishes come close to bowing themselves entirely
out of this book, for most of them have 'no eyes worth mentioning' (see
Fig. 133c). The origin of the cave habit, and the cause of the disappear-
ance of the eyes, are fascinating puzzles however. Cave fishes belong to
many different families and represent many independent invasions of the
cave habitat. All are members of teleostean families in which normal-
eyed fishes occur, though the eyes of these 'outside' relatives are some-
times very small. The North American group of cave forms (the family
Amblyopsidae) have but one non-cavernicolous representative, and the
eyes of this form {Chologaster, in the Dismal Swamp) are much reduced.
Only a very few cave species — notably, several catfishes of the genus
Rhamdia — have kept their eyes in good condition. One, the Mexican
Anoptichthys jordani, was lately shown to contain normal-eyed individ-
uals as well as others showing all grades of reduction of the eye, down
to obsolescence. Such forms have perhaps not long been in the cave envi-
ronment. But, with the possible exception of Anoptichthys, no known

388 ADAPTATIONS TO MEDIA AND SUBSTRATES

cave fishes are believed to have become such through entering caves as
'strays'. On the contrary, much of the evidence suggests that the species
which have taken up residence in caves have ordinarily been well pre-
pared in advance to get along in lightless surroundings :

Many fishes which live in rocky crevices, on muddy bottoms, or in
silty rivers and estuaries, have greatly reduced eyes. Some are even blind,
with a microscopic and sadly imperfect eyeball covered with opaque skin
or embedded deep in the tissues of the head. In such dim-light fishes, as
in many deep-sea forms, the other sense-organs are especially developed,
notably those of the tactual and chemical senses. The animals are thus
well fitted to find food where it is scarce as well as invisible. The an-
cestry of most cave fishes can be traced to such forms. It appears that the
typical cave species is one which has taken naturally to the cave and has
welcomed the refuge it offered — not one which has wandered in accident-
ally and been unable to get out again. Stray individuals of normal-eyed
species are encountered in caves, but many of these belong to groups liv-
ing outside whose way of life, and sensory and reproductive equipment,
would not seem to make them good recruits for the permanent cave fauna.

Tiny-eyed, nocturnal, bottom-grubbing catfishes of several families
have contributed more cave species than any category of outsiders. No
cavernicolous gobies are known, but ichthyologists would not be sur-
prised to discover one at any moment, for many of the 'sleepers' live on
muddy bottoms or in crevices, and have degenerate or obsolete eyes (Fig.
133b). One intertidal species, Typhlogobius calijorniensis, shares its
rocky hideaway with a blind species of shrimp — a pair of the blind fishes
and a pair of shrimps inhabiting each burrow. When adult, the fish is
quite dependent for food upon the activities of the shrimp — almost a
case of the blind leading the blind!

Some especially interesting contributions to the cave fauna have been
made by the family Brotulids. The brotulids are essentially a deep-sea
group. Some species (a couple of them, blind) have secondarily come
to the surface to live on reefs. Still others have made the doubly remark-
able transition to fresh water and the cave habitat — Stygkola and
Lucifuga in Cuba, and another (Typhlias) recently discovered in one of
the caves of Yucatan. In the brotulids, the amblyopsids, various families
of catfishes, and still others, we see clear indications that what has been
called *pre-adaptation' to relative lightlessness can lead to the easy
adoption of the cave habitat. And probably such pre-adaptation is prac-
tically indispensable, if the invasion of the cave is to be successful.

CAVE FISHES 389

Just how the eyes of any blind fish species were led to disappear, we
cannot say. An old idea was that where the eye had become useless, there
was a positive incentive for eliminating the organ, since this would save
energy both in adulthood and — especially — during growth. This notion
seems ridiculous nowadays, for the proportion of a growing animal's
food-intake which goes to enlarge the eye is negligible. Most of the
energy released from food goes for motor and secretory activity, and
only a very small part of the food is converted into new protoplasm.
Nor does the disappearance of an eye leave a hole in the head — its
volume is occupied by tissues (mainly muscle) which consume just as
much energy as the eye had done.

Though a normal eye is excess baggage to a cavernicolous or limico-
lous fish, there appears to be no urgent reason why he should get rid of
it. Useless organs do not always promptly disappear simply because they
have become useless — as witness the human appendix, coccyx, platysma,
tonsils, wisdom teeth, et al. We are left to suppose that in the immediate
outside ancestors of most cave species the eye was 'trying' to disappear
anyway, but was prevented from doing so, by natural selection, because
it was useful and necessary. The usefulness once removed by the assump-
tion of cavernicolous life, the inherent tendency for the eye to shrink was
allowed to express itself, even unto the logical end-result — complete loss.

This explanation does not tax the imagination of ichthyologists as
severely as one might think. In many an open-water fish species, reduced-
eyed individuals appear as soon as the food supply is made abundant
and predatory enemies are removed. Lack of competition then permits
the full development of individuals which, since their germ-plasm has
undergone 'mutations of loss', would formerly have been suppressed by
starvation or capture. Loss-mutations are known particularly to affect
the more complex organs of vertebrates, such as the eye. A species or
family in which such mutations occur with especial frequency has of
course no advantage, over others, in any attempt to become adjusted to
a habitat in which the illumination is reduced or absent. But if a group
which throws loss-mutations also produces an imusual number of other
trial-and-error modifications (as seems likely) , then such a group might
readily evolve the dermal sense-organs, barbels, or whatnot required to
cope with a dim-light environment. Once adapted to dim-light existence,
such a group would actually be better off in a cave, if it happened to
find one, than outside where there were predators to be dodged. And
once inside the cave for good, a rapidly-mutating species would inevit-

390 ADAPTATIONS TO MEDIA AND SUBSTRATES

ably lose what remained of its eyes, though without being under any
positive necessity of doing so. As to whether Rhamdia spp. have only
just found their caves, or are simply slow mutators — the reader may take
his choice.

It is perhaps worth pointing out that even an individual fish, of some
kinds, may be unable to retain useful eyes if kept in darkness. Ogneff,
thirty years ago, kept some goldfish in the dark for three years. At the
end of that time they had lost their skin pigment, their eyes had degen-
erated greatly — though not in any close imitation of those of normally-
blind fishes — and they were quite unresponsive to light. Conversely, it
has been found that in cave salamanders {Proteus, Typhlotriton) whose
larval eyes normally retrogress at metamorphosis to the point of obsoles-
cence, the eyes can become quite normal salamander eyes if the larvae
grow to adulthood in the light. These sightless amphibians thus become
blind in each new generation. No mandatory degeneration of the eyes is
genetically fixed in the species — merely a capacity of the whole eye to
retrogress if it is not used past a certain point in its development, as in
the case of Ogneff's goldfish.

Whether or not the adult ocular degeneracy of any, or many, cave
fishes has a similar basis, is something for future experiments to decide.
And, the cave fishes are but one facet of the general problem of quasi-
eyelessness. Blind, fossorial species are to be seen in every class of verte-
brates except the birds.

Parasitic Fishes — One strange habitat, which is about as lightless as
any, is the interior of an animal. The hordes of internally parasitic inver-
tebrate animals are all eyeless, with the other sense-organs, as well as the
organs of digestion and locomotion, greatly reduced or absent.

A very few vertebrates, all of them fishes, are parasitic. The larger
lampreys are external parasites on other fishes. While clinging to a host,
a lamprey has little need for vision; but since lampreys ordinarily con-
sume only blood, they necessarily spend a good deal of time off of hosts,
engaged in a search for the next victim. Their eyes are important at such
times, for the exploration is largely visual — it has been shown that lam-
preys are attracted to any light-colored object (which could seem to
them to be a fish's belly) moving through the water. They will cling to
a white-bottomed boat, but not to a dark one; and lampreys have given
considerable trouble to human swimmers by mistaking them for fishes.
The eyes of lampreys (Fig. 103, p. 258) are excellent visual organs and
are in no way degenerate.

PARASITIC FISHES 391

The hagfishes, which are the other great division of the cyclostomes
or marsipobranchs, are on the other hand completely blind, their eyes
(Fig. 133a) microscopic and concealed. The hags are internal parasites
of larger fishes — internal predators would perhaps be a better term. They
are extremely voracious and eat everything of their victims except the
skin and the skeleton. While inside a fish, a hag has no more need of
eyes than a tapeworm. In contrast to lampreys, they spend less time away
from a host since they give the latter so much more 'attention'. More-
over, hags are deep-water forms, with admirable tactual and chemo-sen-
sory equipment for locating prey on the bottom by horizontal explor-
ation. They are thus able to dispense with eyes entirely.

One teleost, Simenchelys parasitica, leads a quite hag-like existence.
This entoparasitic eel is most commonly seen emerging from captured
halibut, but it attacks many other large fishes. Simenchelys may prefer
the lightless deep sea, for it has been taken at 2000 meters. The eye is
covered by skin, which in life may be clouded or opaque; but the eyeball
itself may be six millimeters in diameter, and might be called reduced,
but scarcely degenerate.

Still another teleost, the pearl-fish Encheliophis jordani, may be
regarded as an entoparasite or as an internal commensal, depending on
one's point of view. This little fish spends much of its life inside the
cloaca of sea-cucumbers, but it does swim freely in the water at times.
The pearl-fish offers an interesting parallel to Rhamdia and Anoptich-
thys, in that it gives indications of not having long lived in its currently
favorite lightless habitat. The eyes are aimed dorsally, and their circular
pupils are able to contract to mere dots. These features strongly suggest
that Encheliophis, not so long ago, was a free living upward-looker with
habits similar to those of the flatfishes.

Deep-Sea Fishes — After the teleosts crystallized out of the holostean
stock (see Chapter 6), they gradually evolved into a large group in
which a fundamental schism soon appeared. One great, primitive branch
of the class, the Malacopterygii, is characterized by soft fin-rays. The
most specialized division, the Acanthopterygii, derive their name from
their spiny fin-rays. The spiny character has been lost secondarily in
some families whose affinities are clearly with the acanthopterygians.
Other families with soft rays, making up the assemblage called the Ana-
canthini, are sometimes classed with the malacopterygians and some-
times kept apart.

392 ADAPTATIONS TO MEDIA AND SUBSTRATES

Carl Hubbs has pointed out that the acanthopterygians, by and large,
are adapted for a shallow-water, shore existence. They have spread far
and wide into fresh waters, but their marine representatives have mostly
stayed in the littoral zone, on the continental shelves. The malacopter-
ygians, Hubbs emphasizes, are characteristically pelagic. Abundant in
fresh waters and over the continental shelf, they have also been able to
go out into the open ocean, whereas the acanthopterygians are tied to
the bottom. The soft-rayed fishes have retained the primitive connection
of the air-bladder with the throat, and can thus reduce their buoyancy
quickly when they wish to descend for a considerable distance. A few,
e.g., Arapaima, still use it for what was probably its original function —
that of a lung. In the acanthopterygians, the gas-bladder is a blind pouch
and is employed variously as a slow-acting hydrostatic organ, as an ear-
trumpet, or as a resonator for vocalization. Many of these bottom-bound
fishes — the darters, for example — have lost it entirely.

The differentiation of the malacopterygians and acanthopterygians
into originally pelagic and demersal types, respectively, did not remain
at all rigid. Littoral forms belonging to both divisions learned to live
beyond the edge of the continental shelf, farther and farther down the
continental slopes and into the deep water of the bathyal zone. Some
even went out onto the ocean floor, where the depth of the water ranges
mostly between two and three miles. These inhabitants of the abyssal
zone constitute the deep-sea benthos, the bottom fauna. Many families
of fishes are represented in the abyssal portion of the benthos, some of
them having no members elsewhere. For the most part, the abyssal fishes
are archaic.

The benthonic fishes are a minority in the whole deep-sea fish pop-
ulation. A number of pelagic malacopterygians have sunk lower and
lower to become bathypelagic, and a few have even gone all the way
to the ocean floor to become a part of the benthonic fauna. Both the
bathypelagic and abyssal faunas have received new additions from time
to time, and will no doubt continue to do so.

The benthos (but not the richer bathypelagic fauna) contains elasmo-
branchs as well as teleostean species; and of course at one time the only
bathybic fishes were elasmobranchs. A number of rays and sharks, and all
of the bizarre chimaeras, live on the continental slopes and on the ocean
floor. Specimens of the weird luminous shark, Etmopterus (=Spinax)
niger, have been taken at various levels between 100 meters and 3000

DEEP-SEA FISHES 393

The deep-sea fishes thus comprise two distinct faunas; and the dis-
tinction is emphasized by an actual separation. The bathypelagic zone
begins at a depth of about 200 meters where the pelagic zone — which is,
so to say, an extension of the layer of water overlying the continental
shelf — leaves off. Its lower limit is not so definite, but it is probably at
about 2000 meters, and assuredly stops far short of the ocean floor.
Between the bathypelagic and abyssal zones lies a thick intermediate
mass of water in which only occasional wanderers occur. Though the
oceans of the globe contain about 302,000,000 cubic miles of water,
really only a little of this enormous space is inhabited. The sea truly
teems with fish only at the shore and in the waters over the continental
shelves, where such bottom-loving forms as the cod abound.

The deep-sea environment is the closest approach to nirvana that the
earth provides. Below the 200-meter line, which roughly marks the edge
of the continental shelf and the limit of the pelagic zone, the seasons
cease to exist. Below 400 meters, there are no days — only perpetual night.
No plants can grow there, and so it is dog-eat-dog — or dog-eat-carrion,
for a considerable part of the food of deep-sea fishes consists of a ghastly
rain of invertebrate corpses and vertebrate fragments, drifting down to
them from above.

The currents in the deep waters are nowhere rapid, and toward the
bottom the water is quite stagnant over much of the ocean floor — only
the slow Antarctic drift has an influence so far down. The constancy of
deep-sea conditions is reflected in the homogeneity of the fauna, for
about the same assortment of bathypelagic species lives in one ocean as
in another. Only in such enclosed holes as the Sulu Sea, and in the
Mediterranean, have local, unique faunas developed.

The striking features of the bathic environment are the high water
pressure, the low temperature, and the absence of light. Of these, tem-
perature, more than anything else, rules the lives of the deep-sea fishes.
Over about half of the total area of the oceans, the bottom temperature
stands between 35° and 40° Fahrenheit. At depths of 1000 meters or
more, it is usually at the freezing point of fresh water. Near the poles,,
the upper layers of water are extremely cold, but are succeeded by
warmer layers beneath them, and these in turn by the paralyzing cold of
the abyssal drifts. The great 'deeps', scattered here and there over the
globe to the number of about fifty, are well below freezing. Some of them
sound more than six miles, and their waters remain liquid because of the
tremendous pressure.

394 ADAPTATIONS TO MEDIA AND SUBSTRATES

Many deep-sea fishes are really, primarily, cold-water fishes. The same
species, or closely related forms, may live at different depths in different
places, but will be found obedient to isothermal lines drawn through
that whole portion of the sea. Some genera, which are characteristic of
shallow waters in polar seas, are still to be found — living far deeper in
the water — in the temperate regions. Approaching the tropics, some of
these arctic types live beneath two miles or more of water. A few genera,
such as Raja, are found from pole to pole.

To a layman, the most startling feature of the bathic environment is
the hydrostatic pressure. Computations are complicated by the fact that
the weight of a given volume of water increases with depth — the pres-
sures become so great that the water is actually compressed. At a depth
of four miles — and a few fishes exist even there — the water is 3% heavier
than at the surface. Roughly, one ton per square inch is added with each
1000 meters of depth.

Most of us have read popular accounts of submarine rescue work by
skilled divers, and we know that great difficulties are involved in send-
ing a man safely to a depth of even 100 meters in a regulation diving
dress. We tend to assume that if a fish can go blithely down to many
times this depth, he must have some pretty remarkable adaptations to
enable him to withstand the pressure. Yet, during storms, many pelagic
fishes which have no special provisions for it, sink some hundreds of feet
into calmer water, later returning unharmed to their accustomed level.
Though deep-sea fishes cannot be brought quickly to the surface without
their 'exploding', this is because the gases in their spongy remnants of
the swim-bladder, or present in solution in their body fluids, expand when
released from pressure and proceed to blow the viscera out through the
mouth. A fish has no great air-filled chest to be crushed, and so does not
need to be kept distended by an air-compressor at the far end of a hose.
He is not receiving such volumes of compressed air that his blood foams
with nitrogen if he rises quickly, and no excess of oxygen in his brain
makes him light-headed. For him to go downward for a few hundred feet
is not at all the same as for a human diver to attempt to do so. And, for
a surface fish to go down is not at all the same thing as for an abyssal
one to come up (see also pp. 415-6).

Nor does the eye require any special devices for withstanding pres-
sure, though in a captured deep-sea fish it may be bulged from the orbit
by a big bubble of nitrogen which has formed behind it. The tissues of
the eye, and of the whole body, are permeated by a fluid continuum in

DEEP-SEA FISHES 395

which the hydrostatic pressure quickly follows any change in that of the
water outside the animal. As far as the eye is concerned, the principal
adaptations of deep-sea fishes are not to low temperature or high pres-
sure, but to the absence of light :

The transparency of the difFerent seas and oceans varies greatly, chiefly
owing to differences in the concentration of the microscopic plankton
organisms upon which all marine animal life directly or indirectly
depends. A white disc two meters across, lowered parallel to the surface
in mid- Atlantic, is just visible from the boat at a depth of 20 to 30 meters.
In the North Sea, it is visible at such depths only on the calmest days —
ordinarily, it disappears at about ten meters. The light has of course
travelled twice this distance, down to the disc and back to the eye of the
observer. But even making allowance for that, the water at any depth is
dim from the point of view of a fish : he is not looking down at a snow-
white disc as big as a table, but at a dark bottom. Or, he may be looking
horizontally, at objects which receive their illumination glancingly and
reflect very little of it sidewise.

The clearest of all seas is the Sargasso; and even here, the standard
disc can be seen from the surface only when it is less than 66 meters
down. At 370 meters in the Mediterranean, there is not enough light to
affect a photographic plate. In mid-Atlantic, plates were found to be
darkened at 1500 meters — but only after two hours' exposure. An eye,
however sensitive to light, can take nothing but snapshots, and must
have much more light than a camera whose shutter is left open while the
operator goes to lunch. Even well above the 370-meter line, there is in-
sufficient sunlight to affect a retina, let alone enough unscattered light
by which to see — to distinguish one object from another, discriminate
pattern and color, etc.

The deep-sea vertebrates and invertebrates would seem to be in about
the same visual — or non-visual — predicament as the fishes of freshwater
caves. It would not be surprising to find them all completely eyeless. Yet,
not only do a majority of bathypelagic and benthonic fishes have eyes,
but some of them, e.g., Bathylagus, Zenion hololepis, and Epigonus ma-
crophthalmus, have (relatively) the largest eyes of any vertebrates. Few
bathypelagic fishes, however monstrous they may look in a magazine
illustration, are as much as a foot in length; and their eyes never com-
pare, in absolute size, with those of large pelagic fishes or with those of
large land animals. But it will be recalled (see p. 211) that the sensitivity
of an eye does not depend upon its absolute dimensions, but upon the

396 ADAPTATIONS TO MEDIA AND SUBSTRATES

proportioning of its dioptric parts to its receptor surface. The eyes of
deep-sea fishes are probably by far the most sensitive in existence. Some
of them have been claimed to have as many as 25,000,000 rods per
square millimeter of retinal area.

For their ability to retain their eyes and get good use out of them, the
deep-sea fishes can thank their stars. Not their astrological ones, but the
stars that stud their own heads and lie in galaxies along their sides : the
light-producing organs, or 'photophores' (Figs. 137, 139c; pp. 401, 404).
If bioluminescence — the production of cold light by living organisms —
had never been evolved in the animal kingdom, the deep sea would cer-
tainly not be fishless; but its fishes would assuredly be as eyeless as those
of the caves. Excepting occasionally at the surface when there is a great
congregation of luminescent plankton, there is never enough organismai
luminescence to light up the ocean. The great depths, if we could visit
them in a bathysphere, would hardly look to us like a moonlit landscape.
We would be fortunate indeed to see as many 'stars' as are visible on a
foggy night. But when one fish sees from afar the dots or blobs of light
produced by another organism, the recognition of an enemy, or of prey,
or of its own kind — even of its opposite sex — ^may be greatly facilitated.

Great numbers of marine invertebrates are luminous. Of all the species
of cephalopods, about half emit light. Some shallow-water fishes have
illuminant organs, which are sometimes (as in Anomalops and Photo-
blepharon) associated with the eyes (Fig. 134), though whether they aid
the vision of their possessors is questionable. Though the light is perma-
nent, being produced by bacteria confined in a palisade of tiny tubules,
it can be concealed at will by the fish. The pelagic Anomalops swim in
schools, flashing their lights like so many fireflies. Despite the proximity
of the organ to the eye, it is probably only a social signal.

Animal luminescence, as a biological phenomenon, certainly did not
originate in the deep sea; but it has reached its zenith of development
among the deep-sea vertebrates and invertebrates. Beebe has computed
that about two-thirds of all bathypelagic fish species — embracing about
96.5% of all individuals — are luminous. We can be sure that as any one
species of fish worked its way down the continental slope, or slowly
descended from the pelagic zone to the bathypelagic, it would have lost
its eyes but for one thing : in the lightless realm it was invading, there
were luminous organisms which had gotten there before it. The most
ancient of these, at least, must have taken their luminosity down with
them from the surface. In the depths, they found their light-organs val-

DEEP-SEA FISHES

397

uable as lures, as labels, and as aids to courtship. And they kept their
eyes, with which to see the other fellow's lights.

As other species followed into the depths, they too kept their eyes, for
they were never entirely lacking in things to see; and in due course many
of the new-comers developed photophores of their own, if they did not

Fig. 134 — Fishes with light-produdng organs associated with the eyes.

a, Photoblepharon palpebratus, a littoral species from the Banda Sea, showing photophore
(stippled). Based on photograph and drawing from Harvey, b, head of Photoblepharon
sp., profile and section, showing photophore and the opaque 'lid' which can be drawn up
over it. x3. Redrawn from Hein. c, head of the pelagic Anomalops katoptron, profile
and section, showing photophore and the recess into which, after being inverted, it can be
withdrawn, x 3. Redrawn from Hein.

abready have them. But many fishes did let their eyes go to pot. The
deep-sea benthos, particularly, contains many species whose eyes are
covered with opaque skin or are vestigial — e.g., Barathronus, Typhlonus,
Aphyonus, and Tauredophidium among the teleosts, Tyhlonarke, Ben-
thobatis and Bengalicbthys among the rays. The bottom boasts the only

398 ADAPTATIONS TO MEDIA AND SUBSTRATES

vertebrate known whose eyes have gone without leaving any trace what-
ever : Ipnops murrayi. Even this fish has luminescent areas, lying on the
head where the eyes ought to be; and this instance — which could be mul-
tiplied— is evidence that the photophores of a given fish are not neces-
sarily of the slightest use in facilitating the vision of that particular fish.

Among the bathypelagic fishes, there are situations from which one
can deduce something of the usual history of the eye in a species which
invades the depths from the surface. Species which live farther and far-
ther down — say, from 300 to 500 meters — tend to have larger and larger
eyes and more and better photophores. Such forms are obviously trying
to hang onto visual acuity, as well as to increase their sensitivity. Comes
a point, however, at which the eye seems to 'quit', and becomes smaller
once more. The pupil may continue to increase in relative size, accom-
plishing a further increase of sensitivity, but the shrinkage of the eye
indicates that these deeply-living fishes have resigned themselves to
mere light-sense vision. In some deeply bathypelagic forms such as
Cetomimus, Saccopharynx, et al, the eye is vestigial.

These loose relationships of the eye to depth can be seen among
elasmobranchs as well as among the teleosts. The chimaeras of the con-
tinental slopes, and Etmopterus, have big eyes with huge pupils and
vividly brilliant tapeta lucida. The benthonic shark Laemargus on the
other hand has a small eye, and no tapetum; and abyssal rays may be
wholly blind.

Vestigial, blind eyes are more common among the benthonic fishes;
and these for the most part have also failed to develop photophores.
When abyssal forms do produce light, it is usually only a faint glow due
to a special luminosity of the film of slime which covers the body of
any fish.

The deeply benthonic fish is better able to dispense with eyes — and to
get along without photophores — than is the bathypelagic one. Life on the
bottom is largely life in one plane, and the finding of food by touch and
chemoreception is vastly easier. Go far enough along the bottom (if
you're a fish), and you're bound to bump into something good to eat.
But it does so happen that the most conspicuous of the several benthonic
families of deep-sea teleosts, the archaic Coryphaenoidids or grenadiers,
have retained their eyes, which are neither exceptionally small nor un-
usually large.

The retention of eyes by the Coryphaenoididae may be of special im-
portance— not for these fishes themselves, but for some of their descend-

DEEP-SEA FISHES

399

ants. Ichthyologists are coming to believe that the ubiquitous cod family
originated from the grenadiers or 'rat's-tails' — developing a brand-new
tail fin, and coming back up onto the continental shelf. If any blind
abyssal fishes should return to shallow water, they could take up only
habitats in which their blindness was no handicap. It is barely possible
that the reef brotulids, and those which have gotten into caves (p. 388),
were blind before ever they parted company with their many relations
which are still on the ocean floor.

,-<-5J

■(0^(^y-i^

:C'%^^s^-^-^-':S--^.^:'

.■0'.

Fig. 135 — Retinae of bathypelagic teleosts.

a, a stemoptychid, Argyropelecus hemigymnus. X 420. After Contino.
Lampanyctus joubini. x 500. After Verrier.

myctophid,

In large-eyed deep-sea fishes, everything possible has been done to in-
crease the sensitivity of the eye to light. The pupil and lens are relatively
and absolutely enlarged, cones have been largely or wholly eliminated
from the retina, and the rods have been stretched to great lengths (Fig.
135) and enormously multiplied. The retinas of Etmopterus and the
chimaeras have ten or more times as many rods per unit area as do those

400

ADAPTATIONS TO MEDIA AND SUBSTRATES

of the light-bathed, small-eyed rays of the continental shelf. The retinal
photomechanical changes have teen eliminated in adult bathypelagic
teleosts, and the pigment-epithelial cells are often devoid of pigment and
processes. Summation of visual cells in optic nerve fibers is greatly in-
creased (compare Fig. 135 with Fig. 72, p. 177).

The eyeball maintains a substantially normal external form in a ma-
jority of deep-sea species. Such normally-shaped eyes may attain a diam-
eter equal to more than half the length of the whole head, as in Zenion
hololepis. Beyond this point, the relative volume of the eye could scarcely
be increased without serious encroachment upon other cephalic struc-

Fig. 136 — ^Tubular eyes of deep-sea fishes.

a, Odontostomus hyalinus. x 13. After Brauer. ar- accessory retina; cr- chief retina, b, eye
of Argyropelecus sp. superimposed upon outline (dotted) of normally-shaped teleost eye of
the same lens-size. After Hesse.

tures. So, in. many species the 'telescopic' (better, tubular) form of eye-
ball has been evolved:

The relationship of the tubular ocular shape to the normal can be
easily expressed (see Fig. 136, also p. 212 and Fig. 84) : the tubular eye
is like the axial core of a normal eye, the rest of which has been thrown
away to make more room in the animal's head for a very large core. But
in the teleosts the tubular form is not attained, phylogenetically or de-
velopmentally, in any such simple manner. Commonly, both tubular and
normal eyes occur in the same family. Both kinds even occur in different
species of the same genus, as in the bathypelagic genus Evermanella.
In at least some cases (e.g., in Argyropelecus, Ichtbyococcus, Dissom-

DEEP-SEA FISHES

401

ma) , the juvenile eye is normal or nearly so in form, and slowly becomes
tubular during growth (Fig. 137).

In some forms {e.g., Dolichopteryx, Argyropelecus, Opisthoproctus —
Figs. 137, 138a), the optic axis of the adult eye points straight upward.
Here, the lens has moved dorsad and looks through transparent sclera,
not true cornea, the iris and the superior ciliary body disappearing to

Fig. 137 — Development of the tubular eye of Argyropelecus hemigymnus.
X 14. After Contino.

a, 7.5mm. larva — 'praescopic' stage (the eye aims forward), b, 10.3mm. metamorphosing
larva — lens commencing its dorsad migration, c, 10.0mm. metamorphosing larva — lens
continuing migration, d, 7.5mm. postlarval growth-stage — ^final condition (the eye, now
tubular, aims upward); the ventral, pigmented organs are photophores.

allow this. The chief retina, remaining in the floor of the tube, represents
the original inferior periphery of the retina. The optic nerve thus comes
away from the mesial edge of the definitive retina, not from its center.
A portion of the original superior retina often remains, applied to the
lens as an accessory retina (Fig. 136), which is most useful for vision at
a distance (see p. 257). The lens becomes so large that the iris is elim-
inated, the lens itself serving as a pupil. There is little or no possibility of

402 ADAPTATIONS TO MEDIA AND SUBSTRATES

accommodation — the lens is often as big, in proportion to the head, as is
the entire eye of such a fish, even, as ^enion (y.s.).

In such genera as Gigantura and Winteria, where the definitive tubular
eye aims forward (Fig. 138b), similar intra-ocular rearrangements are the
basis of the change in external form. The lens migrates nasally, of course,
rather than dorsally. In Bathytroctes and Platytroctes the eyes are appar-
ently in a half-way stage in evolution toward an eventual forward-aimed,
tubular organ. Bathytroctes is almost unique in having a fovea in its
pure-rod retina (see p. 190).

The utility of the upward aim of so many tubular eyes is not entirely
clear, but it may be associated with the orientation of light-producing
organs. Contrary to common supposition, the luminous organs of nearly
all aquatic animals aim their light downward, not sidewise. This is true
of the many luminous cephalopods mentioned above, and also of the
fishes, both elasmobranchs and teleosts. Where the light comes from a
broad area of skin, as in the luminous shark Etmopterus, this area is
located on the underside. Where there are discrete photophores built like
eyes, with lenses and reflectors, these aim downward — or, if located on
the sides, they are so arranged that 80% of the light goes downward, not
horizontally. There may be a few photophores on the back, but Hubbs
has noted that these are always tiny and often appear to be degenerate
in structure. In the few instances in which photophores shine frankly
horizontally, they differ in numbers and arrangement in the two sexes,
and here they are obviously serving primarily as sexual recognition-marks.

The downward aim of the light seems reasonable enough in a demersal
species; but, it is just as characteristic of the many bathypelagic fishes
which live by day at 200 meters or so and come to the surface at night —
the myctophids or lantern-fishes, the sternoptychids, Astronesthes, Cyclo-
thone, etc. In such vertically migratory forms, most of which school in
large numbers, one might expect the light to be aimed sidewise or even
upward. But whatever the significance of the orientation of photophores
may be, it does seem likely that the upward aim of tubular eyes is in
sympathy therewith. The deep-sea fish is not much concerned with trying
to see objects illuminated by his own photophores — rather, he sees other
organisms by means of their photogenic organs, and his own serve chiefly
as a lure for prey and as an identification-tag for others of his own kind.

The parallelism of the optic axes of all deep-sea tubular eyes, (whether
these are aimed upward, or forward) , in itself poses a special question.
Why should forms with such unsharp vision have such extreme binocu-

DEEP-SEA FISHES 403

larity? Where there is nothing to see but a few dots of light once in a
while, what price such a provision for refined space-perception? Probably,
the binocularity is desirable chiefly because of the impossibility of accom-
modation and convergence in tubular-eyed fishes, coupled with the fact
that the usual monocular cues to distance (p. 314) are lacking in the vel-
vety blackness of the depths. And, probably, binocularity would be just
as useful in the large, normally-shaped eyes of other deep-sea fishes —
but in them, it could not be so easily arranged for. In the creation of the
tubular form, there is opportunity to swing the visual axis through an
exceptionally wide angle. Such forms as Gigantura have simply carried
to a great extreme the same nasad asymmetry which many other animals
have employed as a device for widening the binocular field (see p. 300).

Fig. 138 — Deep-sea teleosts with tubular eyes. After Brauer.

a, with eyes aimed upward (Opisthoproctus soleatus). Redrawn, b, with eyes aimed for-
ward (head of 11.8cm. Gigantura chuni).

If the reader will imagine trying to estimate the distance of a faint
dot of light in a darkroom, with one eye closed, he will appreciate the
value of having bearings on such a stimulus from two angles at once.
The deep-sea fish never has much more to look at than the photophores
of his scanty neighbors. Monocularly, he would be about as helpless to
localize them accurately, as we are to judge the distance of the stars.

Deep-Sea Larval Eyes — Ordinarily the eyes of larval deep-sea fishes
are normal in structure — for larval teleost eyes — and take on any peculiar
conformations, such as the tubular form, during metamorphosis and
adolescence. Here, ontogeny is repetitive of phylogeny. In a few in-
stances, however, this course of events is reversed, and a bizarre larval
eye becomes an orthodox adult organ.

Most outstanding is the case of 'Stylophthalmus paradoxus', a larva
first described by Brauer in 1902. Not until 1934 was it established, by

404

ADAPTATIONS TO MEDIA AND SUBSTRATES

Beebe, that the adult form of this fish is the deep-sea Idiacanthus, known
since the work of Peters in 1876 (Fig. 139). The stylophthalmus larva
has the eyeball at the end of an enormously long stalk, which is sup-
ported by a unique rod of cartilage, rooted on the skull and containing
a muscular insert near its base, which enables the eye to be waved about.
The rod, together with the optic nerve and the filamentous eye muscles,
is ensheathed by skin which (over the front of the eyeball) contributes
to the cornea in the usual way.

Fig. 139 — Idiacanthus fasciola. After Beebe.

a, head of stylophthalmus larva; eye-stalk cartilage shown in black, b, c, 16mm. larva
and adult female; the straight lines under the drawings express the relative body lengths,
d, head of 45mm. postlarva, showing eyes retraaed into head and skein-like, unshortened,
eye-stalk cartilage, e, head of 35mm, transitional adolescent with skin flap raised to show
coiled cartilage in anterior portion of orbit.

In post-larval stages, the eye-stalk shortens to pull the eyeball into
a normal position in the head. The cartilaginous rod cannot shorten,
however, so it bursts out of the stalk sheath and becomes a tangled
skein (Fig. 139d), which is later tucked into the anterior part of the orbit
and covered by the skin of the head (Fig. 139e). The cartilage is even-
tually resorbed during adolescence. The adult Idiacanthus eye is rela-
tively large, but is of normal shape. The male is degenerate, never
getting beyond an essentially post-larval condition except as regards the
reproductive system. Unlike the female, it has a huge photophore on

DEEP-SEA LARVAL EYES 405

the cheek, just behind the eye, which is reminiscent of the conditions in
Photoblepharon and Anomalops (Fig. 134).

There are other stalk-eyed deep-sea fish larvae, notably those of
Bdtbylagus, Eustomias, and certain myctophids; but none can compare
with 'Stylophthalmus'.

In the literature of comparative ophthalmology, one deep-sea fish,
*Scopelu5 caninianus* (= Myctophum punctatum) is erroneously credited
with having 'telescopic' eyes as a larva, the eyes becoming normal in the
adult. The eyes are indeed elongated in this and in some other species
of Myctophum; but the elongation is not axial, but vertical — the vertical
diameter of the eye greatly exceeding the horizontal and the axial diam-
eters, which about equal each other. The eyeball is often pointed
inferiorly, but it always rounds up during metamorphosis. In these
Myctophum species the adult eye is aimed sidewise; but the larval eye
for a time looks directly forward, and thus deserves the adjective *prae-
scopic' equally with Argyropelecus (Fig. 137a), to which this term has
been applied.

The ecological significance of praescopic and stalked larval eyes is
quite unknown. At first thought, one might suppose that they afforded
superior perception of distance through enlargement of the binocular
field or by increasing the length of the inter-ocular base of the range-
finding triangle. But these larvae are only a few millimeters in length, and
their ocular frontality and relatively large inter-ocular distances are very
temporary in the life-cycle, and may have no meaning for binocular
vision — or at least, not the meaning they would have in sizable animals.
Even among large fishes, there are some which only seem to have taken
special pains regarding distance-perception. The hammerhead sharks,
for example, have their eyes very far apart, at the ends of the 'hammers';
but they gaze only laterally, and apparently their monocular visual fields
are overlapped but slightly if at all.

The Common Eel — A really amazing case is that of the common eel,
Anguilla bostoniensis. The biological world was startled when the fairy-
tale life history of this drab fish was finally worked out a few years ago.
One of the most fantastic things about the eel is the cycle of change
through which its eyes pass:

As we see eels during the long vegetative existence of the females in
our inland ponds and streams, their eyes are small, hypermetropic, cov-
ered by a spectacle, and apparently semi-degenerate like those of

406 ADAPTATIONS TO MEDIA AND SUBSTRATES

Necturus. Closer study reveals that the retina is packed with great num-
bers of pseudo-stratified rods, three million of them per square millimeter.
This emphasis on the rods seems surprising; for though Anguilla is noc-
turnal in its feeding, its habits in fresh water would not appear to call for
such an extraordinarily sensitive retina. The eel has even had to manage,
somehow, to make its pupil highly contractile, something which very few
other teleosts have accomplished. Moreover, the chorioid is extremely
thick and the retina is full of capillaries, making it the only vascular
retina which has been found outside the mammals.

The excessive retinal sensitivity and the potentially enormous nutritive
supply have been explained by Franz : they are preparations for a minor
miracle which takes place in a brief period of time toward the end of the
eel's life. The common eel begins and ends its life as a deep-sea fish.
Some months before her one and only breeding period, the eel's skin
turns silvery and her eye rapidly grows until it is relatively huge. The
eye is now emmetropic or possibly even myopic, and its great sensitivity
to light is no more than enough to make vision possible in the next phase
of the life-cycle. The formerly voluminous chorioid is finally justified by
the great ocular growth which has been so rapidly accompUshed by its aid.

The female eels now travel down the rivers to the sea, and they and
the males make their way to the south Atlantic, in the vicinity of the
West Indies. Here the eggs are laid and fertilized, whereupon both of
the parent eels die. The early larvae, which live at great depths (where,
for all we know, the eggs may be laid), develop into the pelagic
'leptocephalus' stage, in which the ribbon-like, glassy-clear fishlet is quite
unrecognizable as an eel. After an extremely slow and largely passive
migration, the baby eel reaches the ancestral estuary as an elver — the
more eel-like stage in which the eels enter fresh water. During the mi-
gration, the relatively large leptocephalus eye must be converted into an
eel eye, thus to remain for years until its time comes to share in its
owner's final preparations for reproduction and death.

Some other fishes develop through a leptocephalus stage : the tarpons,
ladyfishes, and ten-pounders. Some of these may breed in brackish or
fresh water; but none of them passes its adult existence as a small-eyed,
nocturnal, freshwater fish. One leptocephalus (T. mirabilis') has been
found which has tubular eyes. It may possibly develop into some abyssal
species of eel; but the adult has not been identified. The nearest ap-
proach to the whole ocular story of the common eel is that of some
lampreys. Many species of the latter pass through a silvery-bodied,

AQUATIC AMPHIBIA; SIRENIANS 407

large-eyed stage, the 'macrophthalmia', in preparation for their transfer
from fresh water to the sea, where their adult lives are spent. Even in
some of the non-parasitic lampreys which remain always in fresh water,
there are traces of a macrophthalmia stage — as a remembrance of the
more complicated life history of their ancestors.

Aquatic Amphibia — Those salamanders which are permanently
aquatic live in shallow water, and have little use, or special adaptation,
for underwater vision. Many of these forms are secretive, living in mud
or under flat stones — for example Necturus, Cryptobranchus, Siren, and
Amphiuma. In such species the eye is extremely crude and disharmon-
iously developed, and vision is no more than a mere directional light-
sense. As would be expected, the eyes of cave forms (Proteus, Haide-
otriton, Typhlomolge, adult Typhlotriton) are microscopic, concealed,
and functionless. Some newts and axolotls, however, have quite present-
able eyes. Less complex than good anuran eyes, their simplicities are not
all attributable with certainty to the aquatic mode of life. But at least the
spherical lens, the absence of iris folds and of the canal of Schlemm, and
the emmetropic refraction in water are as probably positive adaptations
as they are mere evidences of primitiveness. The few terrestrial salaman-
ders so far studied are emmetropic in air, and hence (at least when
adult) become hypermetropic in water, at breeding time.

In permanently aquatic anurans, such as the aglossal toads (Pipa,
Xenopus, Hymenochirus, etc.) and the pseudine bufonid Telmatobius
microphthalmus, the eyelids never develop as they do, at metamorphosis,
in other frogs and toads. The eyes are very small, with round pupils.
Externally they give the appearance of being almost as degenerate as
those of the Central American termitivorous toads which live under-
ground. But little seems to be on record concerning the anatomy and
histology of the eyes of the above-mentioned genera.

Sirenians — Two groups of mammals have become secondarily adapted
to water so completely that they are even able to breed in that medium
and, unlike the seals, never need to return to the land. These are the sea-
cows and the whales. Not that these animals never put their heads out
of water — supposedly, it was a distant glimpse of an upreared manatee,
its nursing baby cradled in its flippers, which gave some ancient sailor
the raw material from which the legend of the mermaid was constructed.
The old superstition is commemorated in the modern scientific name of
the order Sirenia.

408 ADAPTATIONS TO MEDIA AND SUBSTRATES

The existing sirenians comprise the manatees and the dugongs, the
genera Trichechus and Dugong respectively. These animals are Uttoral,
cropping grasses in shallow water, salt or brackish. In great contrast to
the whales the sea-cows have an acute olfactory sense, and excellent hear-
ing as well. Their eyes are relatively small considering the size of the
animals and the turbidity of their visual medium. The eye of a six-foot
Dugong dugon is about man-sized, with horizontal and vertical diam-
eters of 25mm. and an axial length of 23mm. The eyes of manatees are
somewhat smaller (Fig. 140).

The alterations of the eye for aquatic activity relate chiefly to the
adnexa. While these structures have specialized about as far as those of
whales, the globe on the other hand has lost the organization which
would make it a good organ for vision through air, without taking on
those characteristics which would make it really valuable under water.
As compared with the whales, and particularly as compared with the
seals, the sirenians have been most half-hearted in their ocular mod-
ifications for life in the water — no doubt because they were already
placid herbivores (their ancestral roots are in the pro-ungulate stock)
before ever they took to the sea. The condition of the modern hippo-
potamus, whose eyes are not his pride, affords an analogy for the prob-
able half-way stage in the derivation of the sirenian type from a strictly
terrestrial one (see p. 443).

An unusual area of the sclera shows through the lid opening — as in
man, where it is also the result of a small cornea coupled with great
mobility of the globe. The lids have practically lost their lashes, but
they have well-developed muscles; and a retractor bulbi muscle is present
so that the eye is protectible from mechanical injury. When the globe
is retracted, the lids can be closed ahnost completely. There is disagree-
ment as to whether a nictitating membrane is present. The tear-gland
has vanished, but the Harderian gland has been retained. Its secretion
is apparently not the usual sebaceous sort — Dexler and Freund describe
a continuous flow of tough egg-white-like material from the eyes of a
landed dugong. The cessation of this flow, as in a specimen which has
drowned in a submerged net, promptly leads to a severe damaging of
the cornea by the sea-water. The mucous Harderian secretion is aug-
mented by the products of a regular pavement of special oil-glands lining
the eyelids. Obviously the Sirenia are not interested in trying to recruit
aqueous humor from the outside water, for they effectually prevent the
latter from actually touching the cornea. Like land animals, they secrete

S I REN I AN S 409

their aqueous, with the small number of rugose ciliary processes for
which there is room on the small ciliary body (Fig. 140) .

In sympathy with the 'grazing' habit the cornea is horizontally oval,
being 11.0 x 7.5mm. in Dugong; but this is as far as the eyeball goes
toward the ellipsoidality of full aquatic adaptation (compare Fig. 104,
p. 259). We should expect the eyeball to be flattened — and it is, a bit,
in Trichechus; but it is practically spherical in Dugong. We should also
expect to find a spherical lens close to a broad, flat cornea. Instead,
though the anterior segment is remarkably small, the cornea is arched
and the lens is far from spherical, being the flatter in Dugong. In this
genus, measurements of adult lenses have been given as 6.9 x 4.4mm.,
7.0 x4.0mm., etc. Different investigators have variously computed the

Fig. 140 — Sirenian eyes.

a, a manatee, Trichechus manatus. x 3 !4 . After Piitter. b, dugong, Dugong dugon. xWi.

Redrawn from Pettit and Rochon-Duvigneaud.

quotient of the horizontal and axial diameters of the dugong lens as
1.75, 1.57, 1.25; of the manatee lens, 1.40-1.24. These are hardly ideal
relationships for under-water vision.

Though the lens is very distant from the retina and the visual field
is very large — the eye of Dugong being strikingly human-like not only
in size but in the proportioning of its parts, and with a retinal extent
equalling 265° of the eyeball's circumference — the eye is not as good
an air-seeing one as it looks superficially. Dugong dugon is five diopters
myopic in air, and must be fearsomely hypermetropic in water since it
has no power of accommodation. Rochon-Duvigneaud could not make
out any ciliary muscle at all.

Despite the 'diurnal' gross aspect of the sirenian eye (compare Fig.
140 with Fig. 71, p. 173), it has no devices for high visual acuity. The

410 ADAPTATIONS TO MEDIA AND SUBSTRATES

animals are described as being nocturnal, and their eyes are built for
sensitivity (though there is no tapetum lucidum). The pupil is large,
and is known to react promptly and to have a considerable excursion.
It is said to be displaced ventrally; but its shape is in dispute: it has
been called horizontally oval in both Dugong and Trichechus, circular
in both fetal and adult dugongs, round in living manatees and horizon-
tally oval in dead ones. Except for a few capillaries around the small,
round disc, there are no retinal vessels (as in Rhinoceros) , suggesting a
low retinal metabolism and implying a pure-rod condition or the pres-
ence of but few cones at best. The visual cells have never been preserved
well enough to be described accurately, but the ganglion cells are so few
that summation must be great; and though the optic nerve is thick, much
of its thickness is sheath.

The high sensitivity which doubtless exists is presumably required by
the murkiness of the water stirred up in feeding, but it has been gained
at such an expense of visual acuity that accommodation has been dis-
carded as valueless and even static optical relationships have been
allowed to come undone. All observers agree that the vision of the
sirenians is wretched, and that they pay no attention to visual stimuli
except to withdraw from a bright light. The low value of their eyesight
to them is underlined by the fact that although they almost never look
through air, they actually have less refractive error in that medium than
in water (v.s.). All in all, though the rest of the sirenian body is pro-
foundly modified for full-time marine existence, the eyeball is a dis-
appointment. If we had only the sea-cows to go by, we should be forced
to conclude that the mammalian eye is too set in its ways to depart far
enough from them to give a passable imitation of the eye of a fish.

Whales — The whales have done much better. These great mammals fall
into two sub-orders, the Mysticeti or baleen whales and the Odontoceti
or toothed whales. The Mysticeti have specialized their feeding mech-
anism for straining masses of plankton organisms (largely 'krill', shrimp-
like crustaceans) out of great volumes of water forced through their
plates of baleen ('whalebone') by the inflatable, connective-tissue tongue.
In other respects they are not more highly specialized, except as to size
itself, than the Odontoceti. Although the mysticetes had toothed ances-
tors which were already whales, these were not odontocetes. The extinct
zeuglodont whales do not appear to have been the ancestors of either of
the existing groups of Cetacea, and these ancestors have yet to be found.

WHALES 41 1

The two sub-orders are thus on a par taxonomically, neither being a
derivative of the other. The mysticete eye is definitely less perfectly
adapted to aquatic use than that of the odontocete types; but this is not
because it is more primitive and has departed less far from the ancestral
terrestrial condition. Rather, one must think that the toothed ancestors
of the Mysticeti had better aquatic eyes than their descendants, perhaps
as well adjusted as those of modem odontocetes; and that in the Mysti-
ceti a certain degree of regression has occurred through a loss of impor-
tance of vision, correlated with the evolution of the trawling method of
feeding as opposed to the active visual predation of the squid- and fish-
eating Odontoceti.

The mysticetes run to large size, the pygmy among them {Neoba-
Icena) being twenty feet long and the others — right whales, rorquals, the
humpback, and the archaic California gray — ranging from thirty-three
feet to over one hundred, the two sexes always being about equal. Their
cruising speed is slow, four to six knots; and some are incapable of swim-
ming more than about twice this fast. The great blue whale, largest of all,
is said to be able to swim out of sight in a few minutes; and the finner
(which feeds on herring as well as on krill) and Sei whales are capable
of great speed, the latter having been clocked at thirty knots. All baleen
whales have the habit of sounding, or frequently going to great depths,
rhythmically diving more shallowly and spouting betweentimes. All but
the very largest of them occasionally breach or leap clear of the water,
an action which is purely playful and not comparable with a jack-rabbit's
sky-hop. In fact, it is extremely doubtful if any whale ever puts so much
as its head out of water for the purpose of peering through air. The kill-
ers (Orcinus etc.) among the Odontoceti are credited with thus spying
out the ice floes for potential prey, and the cachalot has been claimed to
stand on its flukes and revolve slowly with the head out of water, sur-
veying the horizon. Identical actions on the part of various mysticetes, at
least, are clearly due to there being insufficient room between the floes
to bring the body up horizontally for spouting, necessitating an uprear-
ing of the head, which may even be rested on the ice for a time.

Among the Odontoceti there is one type, the cachalot or sperm whale
(Physeter) , which imitates the baleen whales in many ways. It is by far
the largest of its group, the male (nearly twice the size of the female)
reaching sixty feet; and it is a slow swimmer — 3-4 knots, 10-12 when
pursued. The sperm whale moreover has the habit of sounding, and has
it even more conspicuously developed than does any mysticete. Physeter

412 ADAPTATIONS TO MEDIA AND SUBSTRATES

holds the records for bodi depth and duration of submergence, for it has
been known to go down, at a speed of eight knots, for more than a mile,
and to stay there for 105 minutes. This performance is related to the
character of the prey, for the cachalot prefers to feed upon the deep-
water giant squid, Architeuthis princeps.

The several species of beaked whales (Ziphiidae) bridge the gap from
Physeter and its pygmy relative Kogia (a latinization of 'codger') to
the great family Delphinidae, incorporating the fifty-odd species of dol-
phins and porpoises. These forms are relatively small, ranging from little
four-foot river dolphins to animals fourteen or more feet long, the very
distinct narwhal and beluga being still larger. The delphinids are pelagic,
and many are notoriously playful. Porpoises are fond of racing against
steamers, and are perfectly capable of keeping up with the swiftest of
the fishes, the 50-knot marlins. Their rolling and frequent breaching is
mere exuberance, and the eye is probably as completely useless in air as
is that of a mysticete. A small, separate family of freshwater dolphins
includes the susa, Pldtanista, already described as having eyes which are
pecuUarly degenerate (p. 210).

Optically, the whale eye has reverted to the fish type — perfectly so, in
the Odontoceti. Otherwise, like that of the Sirenia, it has greeted the
water not as an ancient friend, but as a new enemy. Unable to shake off
all of its previous terrestrial modifications, it has superimposed upon
them still other changes, to make of itself a terrestrial eye secondarily
adapted to water by being shielded from water :

The same glandular pattern that we noted in the sea-cows has also
been independently developed by the whales. Harder's gland is conspic-
uous, and if a lacrimal gland is present it also secretes oil. The sebaceous
Meibomian glands have disappeared along with the tarsal plates in
which they are embedded in other mammals, but the palpebral conjunc-
tiva is paved with small oil-glands. This abundant provision for making
the exposed part of the eyeball salt- and waterproof, and immune to
friction, is aided by the cornification of the corneal epithelium, some-
thing which is seen elsewhere only in the seals, and in one or two ant-
eating mammals — with a different, but obvious, meaning there. The tear-
draining mechanism, sac and duct, has of course vanished. The whales
are the only aquatic mammals which are quite devoid of eyelashes, and
there is no nictitating membrane, no retractor bulbi.

No whale is known to be able to rotate the eyeball, though the extra-
ocular muscles are present and are often quite massive. Their reten-

WHALES

413

tion was once ascribed to their supposed value in keeping the eye warm,
the idea being that all of their contractive effort goes into heat; but this
theory is scouted by recent authorities. The loss of ocular rotability has
had no serious consequences in itself; for the whale eye, situated always
close to the angle of the jaws and thus as much as a third of the way
back along the body (where the head is that large — as it often is) , is quite
incapable of forward vision anyway, to say nothing of binocular cooper-
ation with its fellow.

In many cetaceans, the immobility of the eye can be blamed upon
the enormously thick, stiff sheath of the optic nerve (Fig. 141). When

Fig. 141-

a, a mysticete, Balcenoptera physalis. X Vi; from

b, an odontocete, Phocxna communis. xWi.

Whale eyes. After Putter.

72-foot individual.

vv, vorticose vein.

the eye is immobile, it is only natural that if some particular direction of
vision is most important, the eye should take on a permanent orientation
in that direction. We have seen this to be true in owls, prosimians, and
deep-sea fishes. For the whales, this most important direction appears to
be downward, and the eyeball is canted ventrally or nasoventrally, with
some internal asymmetry which helps out in tilting the visual axis. This
is a prima facie reason against supposing that the whales ever care to try
to see out of water.

The eyelids have altered in sympathy with the ventrad torsion of the
globe. In the odontocetes they are quite equal, for the upper and lower
culs-de-sac have together been shifted to equal extents around the eye in

414 ADAPTATIONS TO MEDIA AND SUBSTRATES

its sagittal plane. The lids are smooth when the eye is open, indicating
that their mobility has been reduced; and complete closure is probably
impossible in many species. Captive porpoises have been observed never
to close the lids completely for more than a few seconds at a time, even
during sleep, Mysticete lids, on the other hand, are less modified. They
are moderately wrinkled when open, and can perhaps be held closed
without strain, though there is no more need for them to be able to close
than in the case of the toothed whales. The upper lid is reduced, but the
lower is puffy; for, the fornices have not shifted to let the eye aim down-
ward as readily as in the odontocetes.

Going with its general superiority over the mysticete organ, the odonto-
cete eye has the pupillary operculum much better developed — this being
in sympathy with the predominant importance of the lower visual field,
as is also the dorsal location of the tapetum lucidum in all whales. The
operculum is actuated by intrinsic muscles, in contrast to the pupillary
opercula of fishes — whose modus operandi is unknown, but which at
least are known to contain no muscles. The internal shape and arrange-
ments of the cetacean eyeball are strikingly fish-like (Fig. 141), except
that it has not gone in so strongly for periscopy. The ovoid cornea is
small in area, particularly in mysticetes, which by some is considered an
adaptation for the conservation of heat. In the toothed whales at least,
the cornea is greatly thickened at its margin, as in elasmobranchs and
many teleosts. The eye is horizontally ellipsoidal, which helps to extend
the horizontal visual field. The antero-posterior axis is enabled to be short,
by the hardness and relative smallness of the lens, which has a refractive
index approaching that in fishes. In odontocetes the lens is often a per-
fect ball, and never has an equatorial diameter more than 1.2 times its
axial diameter. In whalebone whales the lens is at least this much flat-
tened, and may have an equatorial diameter as much as 1.5 times the
axial. In keeping with these differences, toothed whales have flatter,
hence more fish-like eyes, the axis being six-tenths of the vertical diam-
eter; while in mysticetes it is seven- or eight-tenths.

The Odontoceti have powerful ciliary muscles, sometimes even with
some circular fibers as well as radial ones. Baleen whales may have no
ciliary muscle at all, and never have more than from one-half to one
diopter of accommodation. In compensation, they have even longer rods
in their retinae than the very long ones of odontocetes, though this differ-
ence undoubtedly exists primarily to increase sensitivity, in those whales
which sound to almost lightless depths. It does not appear to be known

WHALES 415

whether Physeter has extra-long rods compared with other genera of its
group, most of which are shallow-swimming forms.

The most striking thing about the whale eye, as the reader's first
glances at the illustrations must have shown him, is its phenomenally
thick sclera. It results in the eye having actually a relatively small inter-
nal volume. Beer was unable to learn of a whale eye with an internal
capacity of more than 123 cc, though whale eyes may be several inches
in diameter; whereas the 37-millimeter eye of an ocean sun-fish (Mold
mold) which he measured would hold 180 cc. The thick sclerotic coat
and optic nerve sheath (Fig. 141) are generally assumed to be adaptive
to the resistance of the water pressure endured by the sounding cetacean.
The same thick sclera is seen in the monstrous (65-foot) whale shark
(Rhineodon typus) and in the (also huge) basking shark (Selache max-
ima)— and the latter, at least, goes to great depths. But it is again seen
in the elephants, which seldom get their heads wet.

Adaptation to Water Pressure? — The generalization has been made
that animals which are very large for their kind, and whose eyes are
relatively small for their size, have extremely thick scleras. In such forms
as Cryptobranchus, possibly also in the European sturgeons, we can
shrug this off as a 'disharmony'. The eyes of elephants, large sharks, and
whales are too well built to make such a dismissal plausible. The thick
sclera is seemingly really necessary, to maintain ocular rigidity against
the pull and haul of the extra-ocular muscles. For, the absolute strength
of a muscle increases as the cube of its linear dimensions; and when an
object is greatly enlarged without a change of its material, its rigidity
declines. A plank in the proportions of a toothpick would be far more
supple than the toothpick itself.

But the whale eye, though it may be as large as a grapefruit, is sup-
posed not to move. Does the water-pressure theory then account for its
extra-thick rind? The scleras of deep-sea fishes are not thick, but we tend
to suppose that these animals are somehow adjusted to the hideous pres-
sure bearing upon them (see p. 394). In actual fact, no fish needs any
sort of adjustment to meet great pressures, for there is an incompressible
fluid continuum throughout his tissues, whose pressure at all times equals
exactly that upon the body surface. Any surface fish which can stand
cold water, and whose anatomical topography will tolerate having the
swim-bladder completely collapsed without ripping anything among the
viscera, can plunge slowly for a mile or for as many miles as the deeps
provide. He would have to be slightly insane to do so, he might have a

416 ADAPTATIONS TO MEDIA AND SUBSTRATES

Struggle to rise again until the refilling of the gas-bladder had restored
his buoyancy, and he might have to rise slowly to avoid the equivalent
of caisson disease, due to warmed, decompressed gases foaming his blood.
But he would take no harm.

The eye is in even better position (than the body as a whole) to
'stand' this pressure which does not have to be stood; for it contains no
air-pockets whose compression to the point of obliteration would cause
distortion. The whole body of a sperm whale must have a tremendous
problem in keeping half-a-million tons from collapsing his lungs. Indeed,
the diaphragm may somehow permit such a collapse, the viscera coming
up into the chest cavity and squeezing so much oxygen into the blood
that the animal's ability to remain so long below, and his necessity for
spouting sixty times before he can sound again, are thereby accounted
for. But the whale's eye certainly does not need its thick sclera just be-
cause the beast subjects himself to a great range of pressure :

Etmopterus can live as deeply as any whale ever goes; and in a speci-
men of this shark whose eye measured 17.0 mm. in diameter, an inves-
tigator found the sclera to be microscopically thin. In the benthonic
chimaeras, the sclera is actually discontinuous. In bathypelagic teleosts
the scleral cartilage has been reduced from the usual extensive cup to a
narrow ring. When all of these fishes which face great pressures, and
great changes of pressure, have weaker eyeball-walls than their shallow-
water relatives, it hardly looks as though the whales needed to thicken
their scleras for pressure-resisting purposes.

The mere fact that the whale's cornea is relatively thin — though com-
pletely exposed to the water — is by itself enough to show that the thick-
ness of the sclera can have no relation to high pressure as such. But the
differential pressures upon various areas of the cornea, due to wave
action, to ordinary swimming movements, and to quick changes in speed
and direction, would deform so thin a cornea on so large an eyeball,
were that cornea not supported peripherally by an immensely stiffer
structure — just as a plastic watch-glass is supported by its unyielding
metal bezel.

While a grape keeps its rotundity nicely while lying on a table, it
would flatten out and burst if it were magnified to the size of a house —
unless, that is, its skin were thickened out of proportion. The inordin-
ately thick scleras of the large whales and the biggest sharks are no
thicker than need be. They are a logical result of making a soft-tissued
optical instrument almost too large for rigidity in the face of the buffet-

ALTERATIONS FOR AERIAL VISION 417

ings of the severe aquatic environment. The great whales would still
need their thick scleras, even if they never left the surface at all.

Scleral cartilage has been allowed to disappear in all vertebrate groups
which have allowed the eyeball to become spherical — in salamanders,
snakes, and mammals. Where, as in the large whales, the globe has later
ballooned and flattened, the sclera has had to be thickened very greatly;
for it takes a deal of connective tissue to give the same stiffness as a
much thinner piece of cartilage. It was a great piece of luck for the
vertebrates to chance upon the plan, for their eyes, of a membranous
sac kept turgid by internal fluid pressure. The whales have crowded that
luck about as far as can safely be done.

(B) Aerial Vision
The emergence of the vertebrates upon the land necessitated several
changes in the eye, which in turn made possible certain improvements
which would never have been brought about in the water. Some of these
changes (those of the eyeball itself) were mostly related to the major
optical difference between air and water — the difference in refractive
index. Other changes (those in the adnexa) were demanded by the loss
of the moistening and cleansing action of water, and by the new jeopardy
from sharp blows and abrasive objects.

Changes in Dioptrics — The alterations of the eyeball for vision
through air were essentially optical. No longer was the eye shielded
from harmful ultra-violet light, and the lens and cornea had to become
able to absorb this light, or to change it by fluorescence into harmless
visible light. No longer could the cornea with impunity have an irregular
surface, and with the Amphibia it becomes smooth and optically perfect.
Nor was a flat corneal surface any longer necessary or desirable. Exposed
to air instead of to water, it became the most important refractive surface
in the eyeball, where it had formerly been a nonentity. When the cornea
became arched, as it first did in the amphibians, this drew the optical
center of the eye forward. This in turn enlarged the image, even though
the lens, now relieved of the lion's share of image-placement, became
flatter and receded into the eye (cf. Figs. 105 a and 106; pp. 261, 266).
The backward shift of the lens was of inestimable importance for the
future, for it placed the lens in such a relation to the ciliary body that
the latter could eventually (in the Sauropsida) take over the labor of
accommodation, and could accomplish this adjustment with greater
speed, and over a far greater range, than had hitherto been possible.

418 ADAPTATIONS TO MEDIA AND SUBSTRATES

New Extra-Ocular Structures — Associated with the typical fish eye
there are only the standard oculomotor muscles and a circular lid-fold
rimming the orbit. The immobile lid-fold is simply the margin of a
circumocular sulcus, which is lined with a conjunctiva containing mucous
goblet-cells (which persist into the mammals), but without massive
glands of any kind. On taking to the land, the vertebrates were able to
develop sharper vision by reason of the greater amount of light available,
making possible an increase in the relative number of retinal cones. But
while vision through air meant better vision, it also meant exposing the
eye to desiccation which would ruin it for optical purposes and leave it
an easy prey to infection. On land, too, there was a new danger of injury
to the eye from dry, hard, windblown particles and from sharper col-
lisions of all sorts than are possible in the cushioning medium of water.
The vertebrates' first solution to these new problems was the production
of fluid-secreting structures (the ciliary processes) inside the eyeball, and
of two or more lids, new glands and new muscles outside it. In some
animals this artificial aquatic environment of the cornea proved inade-
quate for its protection, and there was manufactured a still more perfect
shielding device, the tertiary spectacle (section D) .

Adnexa in Amphibia — It was pointed out in the preceding section
that the great majority of Amphibia are not amphibious, but are aquatic
as larvae and terrestrial as adults. The adult amphibian, then, has need
of about as complete a set of protective adnexa as does any land animal
which never goes near water. If the terrestrial Amphibia fail to show
such an elaborate array of ocular glands as higher forms possess, one
should not be too ready to attribute this solely to primitiveness; for,
after all, they mostly remain in damp situations even though on land.
Salamanders are to be found in such situations as on the moist, cool soil
under fallen logs. Frogs sit at the water's edge or move about in the
humid air at the grass-roots of waterside meadows. Spadefoots may be
very numerous in a locality, yet never seen until a prolonged rainstorm
brings them out — the basis of one of the several legends of 'rains of
frogs'. Other toads, and tree-frogs, may be found in the driest of places
— but they are careful to keep out of the sun. Toads often burrow
through dry soil into earth which is not so dry. If the skins of amphibians
had permitted them to adopt drier environments, we may be quite sure
that the ocular adnexa would quickly have gained the complexity shown
later by the scaly sauropsidans.

ADNEXA IN AMPHIBIA 419

Permanently aquatic salamanders and frogs, and the larvae of all
amphibians, have no lids or special ocular glands. In adult land sala-
manders a distinct, thick skin-fold forms an upper lid and a thinner,
mobile lower lid is present. Its transparent border moves upward to close
the eye, and the lid is lubricated by a row of compound glands in its
lining. These may be best developed nasally and temporally; and the
intervening glands may even be lacking, so that two masses of glands
are isolated — the forerunners of the serous lacrimal gland (temporally)
and the sebaceous Harder's gland (nasally) .

In the anurans the transparent portion of the lower lid has been elab-
orated and is retractible within the remainder to form a Z-like fold
(Fig. 106, p. 266) — often loosely termed a 'nictitating membrane' though
it has no phylogenetic connection with the true nictitans of higher forms,
or with that of the requin sharks. The thickened rim of the lower lid
continues completely around the posterior of the eyeball as a cord, which
passes through the retractor bulbi (see Fig. 143a, p. 421). When this
muscle contracts, the eyeball is pulled into the head and forms a bulge in
the roof of the mouth, which is of considerable aid in the swallowing of
food. The resultant tug on the cord pulls out the fold of the lower lid
and slips the latter up over the cornea to meet the motionless upper lid.
A broad hammock-like muscle behind the eye, the levator bulbi, raises
the globe once more to its normal elevated position and the lower lid
automatically slips down into its folded attitude. The eye can close with-
out complete retraction; but the retractile closure, and the muscles con-
cerned, are important for protection against mechanical pressure and
blows. The frog having no flexible neck, the eye must be able to dodge,
since the head as a whole cannot! The single large gland present is con-
sidered to be the Harderian, and spreads into the orbit at metamor-
phosis to take a position among the muscles behind the eyeball. There
are apertures, at the middle and at the nasal end of the lower lid, which
communicate with a nasolacrimal or tear duct. This tube lies chiefly in
the skin and runs horizontally to the small nasal cavity.

The permanently aquatic anurans (see p. 407), as might be expected,
have secondarily lost the lids, and probably most or all of the special
muscles and glands developed by terrestrial amphibians. The adult eye
still peers through the primary spectacle of the tadpole.
The Third Lid and the Fate of the Retractor — In the Sauropsida,
the lower lid still characteristically does all the work of closing the eye;
but being thicker than in the frog, and moreover rendered opaque as a

420

ADAPTATIONS TO MEDIA AND SUBSTRATES

rule by scales or feathers, its action results in a brief period of blindness.
A third lid, the vertical 'membrana nictitans', has consequently evolved
as a fold of the conjunctiva at the inner or nasal comer of the lid
opening (Fig. 142). Being transparent, it can sweep the cornea from
the nasal to the temporal side, to clean and moisten it, without shutting
out the light. This action is of paramount importance to the scampering
lizard or to the bird in flight, exposed to a stream of air which would
quickly dry the cornea. There are many ornithologists who believe that
the nictitans is held over the eye most or all of the time that a bird is
in the air — the forerunner of the motorcyclist's goggles. The retractor
bulbi muscle remains important in the reptiles and persists into the
mammals. In mammals, as in the dog and cat for example, it is often
divided into four slips alternating with the rectus muscles. It is lacking

Fig. 142 — The nirtitating membrane or third eyelid. From Wolff, after Sutton.

a, b, front and rear views of turkey eyeball with nirtitans, its tendon, and the muscles
which operate it. x 1. c, the mechanism in situ in a disserted head.

in birds — the bird orbit hardly ever affords enough room for the retrac-
tion of the large avian eyeball, and the flexibility of the bird's neck is
adequate compensation. In man, it is the heavy bony rim of the orbit,
particularly the ridge bearing the eyebrow, which makes a retractor bulbi
unnecessary. We may be 'hit in the eye' by a swift baseball, without the
eyeball necessarily being harmed. Our erect posture may also have some-
thing to do with the loss of the retractor, which obviously is of greatest
value to those large-eyed forms which, like the horse, hang their heads
for a good part of the time, when feeding.

Adnexa in Sphenodon — In Sphenodon, the most generalized of liv-
ing reptiles, the lacrimal gland is lacking; but a large Harderian gland
moistens the cornea and lids adequately with its oily secretion. The

THE NICTITANS; ADNEXA IN REPTILES 421

lower lid contains a tough tarsal plate which stiffens it and makes it slide
smoothly. The nictitans contains a supporting cartilage, and its free
edge continues ventrally as a cord or tendon around to the back of the
eye (Fig. 143 b). Here it is attached to the retractor bulbi, hence is pulled
upon whenever that muscle shortens. The cord continues to an attach-
ment on the dorsal wall of the orbit. The horizontal nasolacrimal duct
has two openings or punctae lacrimalia, on the lower-lid margin, one at
the nasal end and the other several millimeters laterally from that point.

Fig. 143 — Musculature of the nictitating membrane in various vertebrates. After Franz.

a, frog, h, Sphenodon. c,\izatd {Lacerta). d, alligator, e, turtle, f, bird. B,B(Q)-
bursalis or quadratus muscle; B. r.- retraaor of bursalis; n- tendon to nictitans; N- optic
nerve; p. «.- tendon to lower lid; Pyr- pyramidalis muscle; R. b.- retractor bulbi muscle.

Crocodilians — The crocodiles and their allies have gone back into the
water, but they had previously developed a full panoply of terrestrial
ocular accessories. They are exceptional among the reptiles in having the
upper lid the larger and the more mobile, as it is in mammals. Corres-
pondingly, the upper lid usually contains a (bony) tarsus. A cartilage-
like one is present in the nictitans, but there is none in the lower lid. The
large nictitans has developed a 'pyramidalis' muscle in its own tendon
(Fig. 143 d), which inserts on the back of the eyeball itself instead of on
the orbital wall as in Sphenodon — a change which keeps the nictitans in
a more nearly constant relation to the eyeball during eye movements.

422 ADAPTATIONS TO MEDIA AND SUBSTRATES

Though it is difficult to see how the pyramidaUs could have arisen as a
derivative of the retractor bulbi, it is supplied by the same cranial nerve,
the sixth or abducens. In fact, all of the conspicuous muscles specially
developed by land animals — retractors, levators of the upper lid, depres-
sors of the lower, operators of the nictitans — are irmervated by one or
another of the same three cranial nerves (third, fourth, and sixth) which
supply the six primitive oculorotatory muscles (the four recti and the two
obliques). Each of the newer muscles can be seen, with more or less
clarity, to have been derived from some member of the original set.

The crocodilians have a lacrimal gland under the dorsal orbital roof —
the lacrimal, in vertebrates generally, is most often tucked under the
more mobile of the two lids — and they also have a large Harderian gland
with several outlets beneath the nictitans. This situation reflects the
greater importance of oily, than watery, secretions for the insulation
of an essentially terrestrial eye, in an animal which has secondarily
returned to water. The condition in the marine Crocodilus porosus is
particularly interesting, as a parallel to that in the Sirenia and Cetacea;
for here the conjunctiva of the lower lid is similarly paved with glands,
and the nasolacrimal duct, though present, has only one puncta instead
of the row of three to eight seen inside the lower lids of other crocodiles.
In Caiman sclerops (the spectacled cayman) the upper lid shows peculiar
variations, being swollen and wrinkled in some individuals and horny in
others, as it is also in C. latirostris.

Turtles — The turtles have also 'gone back to the water', and their eyes
reflect the change of habit from terrestrial to amphibious — and back to
terrestrial, in the box turtles and desert tortoises. The adnexa have fol-
lowed all but the last of these vicissitudes.

The lower lid is the larger, but has lost its tarsus since the wetted eye
needs none. The nictitans has a small cartilage and is operated, as in
crocodiles, by a pyramidalis, which sends a second tendon to the lower lid
and thus acts as a levator muscle for the latter (Fig. 143e). The retractor
bulbi is powerful, and may turn the eyeball almost completely over as it
retracts, the nictitans and lower lid closing the eye passively at the same
time. The palpebral fissure, or opening between upper and lower lids, is
canted more or less so that it runs dorso-temporally to ventro-nasally of
the eyeball. Though this same slant has been retained in strictly terres-
trial turtles, it seems most useful to the freshwater and marine turtles,
which float in a slanted position at the water surface; for when their

ADNEXA IN REPTILES 423

heads are thrust upward into the air, in line with the axis of the body,
the palpebral fissure is then actually parallel to the water (see Fig, 160b,
p. 547).

The lacrimal gland shows much variation. It may be compact with
one or many ducts, or scattered along the length of the lower lid as in
salamanders. The Harderian gland is present, with a single duct, and
the nasolacrimal duct is completely absent in all turtles. A real puzzle is
the enormous size of the lacrimal gland in the marine turtles which, one
might think, should need none at all. It may be needed during visits to
land for egg-laying; and, since males of the marine forms are rarely
caught, it is not on record whether the gland is much smaller in that sex.
Or perhaps the secretion is mucous or oily, and affords an analogy with
the marine mammals — no one seems to know.

Lizards — In the lizards, again only the lower lid has a tarsal plate and
moves, as a rule. In one anole, at least (Anolis alligator) , the two lids
do move equally. The lower lid is operated by a muscle somewhat like
the orbicularis oculi of the mammals (Chapter 2, section C), but of
course is not homologous therewith, since the mammalian muscle is a
derivative of the facial platysma peculiar to the class. The tendon of the
nictitans is enfolded by the peculiar 'musculus bursalis', from which a
special retractor muscle runs to the sclera to keep the apparatus from
pressing on the optic nerve (Fig. 143c). These new muscles are supplied
by the sixth cranial (abducens) nerve.

The Harderian gland is large, lies nasoventrally alongside the globe,
and has a single duct. The lacrimal gland lies at the temporal canthus
of the palpebral fissure and has several contractile apertures. It is lacking
in some lizards, notably the chameleons. These aberrant forms have no
nictitans, and have the palpebral fissure greatly reduced to about the
size of the pupil, the lids clinging as a broad circular fold to the surface
of the huge eyeball, and turning with the eye. They seldom close except
in sleep; but when they do, they meet along a straight line as usual. This
situation might have arisen from one similar to that in some other
lizards, for instance the family Agamidae, where the upper and lower
lids merge into one another at the canthi (as they do also in toads) . In
several lizards, and two turtles as well, the lower lid shows a special mod-
ification to permit vision with the eye closed, and in some burrowing and
nocturnal forms the palpebral complex has been frozen into a permanent
spectacle, like that of the snakes.

424 ADAPTATIONS TO MEDIA AND SUBSTRATES

Snakes — The snakes show a maximum of modifications, of which the
spectacle (Fig, 154, p. 456) is the most conspicuous — the others being
consequences of its presence. The lacrimal gland has disappeared, and the
enormous Harderian gland lies beneath and behind the eyeball. Its duct
opens directly into the nasolacrimal canal, which has a single aperture
(spectacled lizards have two) in the conjunctival sac, at the nasal side.
As in the lizards, the distal end of the nasolacrimal duct opens within
the nasal cavity, inside the accessory olfactory Vomeronasal organ' (of
Jacobson). The Harderian secretion then proceeds to the mouth cavity
and contributes substantially to the saliva, which in snakes must lubricate
the prey thoroughly for swallowing. Rudimentary-eyed snakes such as
Typhlops and Rhinophis have even lost the connection of the nasolacri-
mal duct with the conjunctival sac, and the Harderian duct opens into
the mouth independently of Jacobson's organ, to facilitate still further
the strange function of the Harderian gland as an accessory salivary
organ.

Birds — In birds, the lid opening reveals only the small cornea, so that
one is easily misled as to the true size of the eyeball, and receives
quite a shock upon skinning a bird for the first time! In this class of ver-
tebrates, mobility of the upper lid reappears, in nearly half of all species.
Most of these are in the higher orders, the ostrich being a conspicuous
exception. The lower lid has a fibrous tarsus (except in parrots) , but the
nictitans has none, and is more perfectly transparent than in reptiles
(except crocodiles, where its exceptional clarity would seem to go with
nocturnality) , In the owls and dippers, however, the nictitans is cloudy.
Its inner surface is always covered by an epithelium whose surface cells
are built like unicellular feathers, which improve its cleansing action.
These, incidentally, are imitated in some lizards by peculiar epithelial
papillae; and the lizards have produced imitation hairs as well as feathers,
for some (e. g., Eublepharus, Coleonyx) have 'eyelashes', manufactured
from scales.

A large bursalis is present but the pyramidalis has been retained, not
abandoned as by the lizards — if indeed they ever had one (Figs, 142 and
143f). The nictitans- tendon may have a very long path, because of the
breadth of the globe equatorially, to reach the muscles which operate it.
In the owls the eye is so long, and the orbit so snug, that the tendon
courses along a groove, and over a pulley, on the surface of the eyeball
(Fig, 144). As in most reptiles, the lids can be closed without the eye

ADNEXA IN BIRDS AND MAMMALS 425

retracting; but here it is because the orbit affords no room at all for a
retractor bulbi.

The lacrimal gland is ventro-temporal in location, with a single duct
which opens inside the lower lid. From bird to bird it shows what seem
to be inconsistent variations. It is minute, as might be expected, in one
group of amphibious birds (the penguins) but is particularly large in
another (the dippers or water-ouzels). The owls lack it, and moreover
have a very small Harderian gland, as do also their remote ancestors the
goatsuckers. The very large Harderian gland
of the cormorants makes good sense, for these
are marine amphibious birds; and the avian
Harderian secretion is a thick, oily emulsion
which, if abundant, would shield the eye well
from the osmotic and chemical effects of sea-
water. In birds there are two slit-like punctae at
the nasal canthus, the upper one being the
larger of the two. The penguins appear to have
lost the nasolacrimal duct, for their oily tears Fig. 144 — Ventral view of
are described as spilling down their cheeks tt, ZwrnUTci.t'it

when they are out on land. and its pulley. After Franz.

Mammals — In the mammals, the upper lid ordinarily comes down much
more than the lower comes up. Exceptions are the elephant and hippo-
potamus, the camel and reindeer, the great elephant-seal, and a number
of very small forms, such as the mouse. Both lids, or only the upper, may
have tarsal plates. The monotreme echidnas carry out their generally
sauropsidan-like ocular makeup by having a tarsus in the lower lid alone.
The two lids in mammals are approximated by the annular 'orbicularis
oculi' muscle, which sweeps around through both like a flattened dough-
nut (Fig. 17, p. 39). They' are separated largely by the actions of the
levator of the upper lid (a derivative of the superior rectus, which it
parallels) and of the more intrinsic depressor muscle of the lower lid.
In many forms, particularly primitive ones, the lids are thick and their
action slow; but ordinarily they are thin and the 'blink' may be lightning-
quick like the movement of a bird's nictitans. Except in forms whose
binocular fields are very narrow (like the rabbit), the lids of both eyes
react when only one pair is stimulated. We have all seen humans who
have never learned to wink one eye!

426 ADAPTATIONS TO MEDIA AND SUBSTRATES

The Meibomian glands, embedded in the palpebral tarsi, appear in
the mammals for the first time. They could not well have evolved sooner,
since they represent glorifications of the oil-glands associated with hairs.
They are lacking in some species; and true eyelashes are absent in the
elephants and whales, nearly so in the sea-cows and hippopotami.

The lacrimal gland lies near the temporal canthus. Associated as
always with the more mobile of the lids, it may lie wholly above this
level and has most of its 1-15 ducts opening under the upper lid. It is
usually lobed or divided, as it is in man. In murid rodents it is tiny or
lacking, though Harder's glands (and other glands, peculiar to rodents)
are present, Harder's gland sometimes being very large and forming a
cushion over the whole back half of the eyeball (mice; also, shrews).
The lacrimal is said to be lacking in the pronghorn, Antilocapra ameri-
cana. In the pig its secretion is not watery as usual, but is rich in mucus.
The drainage canal is vertical and opens by two punctae, one on or near
each lid-margin at the nasal canthus, with a caruncle (Fig. 16) usually
lying between them.

The nictitans has its ups and downs in the mammals. Where it is well
developed, it usually has a cartilaginous tarsus, but it never has a special
musculature behind the globe as in lower vertebrates. Hence, it slips over
the eye only passively when the globe is slightly or markedly retracted.
Contrary to logical expectations, it is most rudimented in the lower mam-
mals and has come back to greatest usefulness in some of the higher ones.
This probably explains the absence of its characteristic muscles, these
having been discarded in early mammals to whom the nictitans was un-
important. It is present in the duck-bill but lacking in the echidnas, and
it is vestigial in rodents and others of the lower orders such as the insec-
tivores, primates, and 'edentates'. One of the latter group however, the
aard-vark (Orycteropus) , has a nictitans which is on a par with that of
the horse — ^probably as a protection against the termites on which the
beast feeds. The scaly ant-eaters (Manis) also have it decently developed.

All carnivores except the skunk, whose eye protrudes greatly like that
of a mouse, have a nictitans. All can move it, though not all ever do so.
In only a few could it possibly be drawn all the way over the cornea, the
'haw' of the domestic cat being a familiar example of this rare degree of
development. In bears, the nictitans is not ordinarily moved, but it drifts
partway over the cornea when the animal becomes sleepy. The same
reaction is seen in the rhinoceroses. The white bear, however, has an
excellent nictitans, and uses it as a defense against snow-blindness (as

ADNEXA IN MAMMALS 427

does also the reindeer). The bear-like giant panda also has a prominent
nictitans.

Ungulates all have the nictitans, though with great interspecific vari-
ations, and usually with no apparent usefulness. In the horse family,
however, the nictitans is as extensive and as rapid in action as in many
sauropsidans. Its retention here is attributed to the need for special pro-
tection of the eye when feeding in deep grass, and an analogous useful-
ness would explain its persistence in the Sirenia. It has however not
been reported as being particularly well developed in the antelopes, most
of which have horse-like feeding habits.

The retractor bulbi is well distributed in the lower orders of mammals,
and occurs in scattered species among the higher orders. In some mam-
mals, including all rodents, the globe is pulled back somewhat into the
orbit directly by its action. In other instances, especially among the
'edentates', the eye seems rather to be pressed back passively by the lids
during their periodic closures. In the hairy armadillo (Dasypus villostis) ,
and also in the echidna, the lids simply swing together like a pair of
gates whenever the eye is retracted, instead of sliding over the globe.

A most peculiar arrangement is seen in the opossum. As the eye closes,
two vertical folds form in the conjunctiva, one at either canthus; and
these close tightly over the cornea so that if the lids were then forced
open, one might think the eye had been replaced by a white tumor. The
writer has been fooled by a similar concealment of the retracted and
rotated eyeball of a snapping turtle by proptosed conjunctiva and mus-
cles. Another unusual phenomenon occurs in the rhinoceroses and, less
conspicuously, in one species of bear {Melursus labiatus) . Here the eye-
ball, every few seconds, is flicked temporally and retracted at the same
time, all with lightning speed. The action appears to be a clumsy sub-
stitute for the kind of rhythmic blinking we humans perform, for it takes
place too quickly to seem a means of sweeping the horizon for the detec-
tion of possible approaching enemies,

Inter-Relat'wns of Globe and Adnexa — The evolution of lids and
their associated muscles and glands by the air-breathing, air-seeing verte-
brates represented primarily an effort to protect the eye by keeping it in
a local aquatic environment. This method has been highly successful —
too much so, in a sense, in secondarily aquatic forms, which have appar-
ently found it impossible to dispense with as many of the concerned parts
as we might think they could easily discard. An even better protection

428 ADAPTATIONS TO MEDIA AND SUBSTRATES

of eyes exposed to air and to injurious terrestrial objects has been pro-
duced, in the form of a tertiary spectacle (section D), in some verte-
brates— but unfortunately only in those which were absolutely driven to
make this logical modification of the mobile palpebral system.

But the lids have not been without their purely optical influences upon
the eyes of land animals. The very choice of an upper-lower combination
instead of a nasal-temporal or diagonal one (the turtles excepted) was
dictated by the predominantly vertical direction of the incident sunlight.
Again, as long as the animal's eyes were carried close to the ground and
exposed to bright upward reflections from the substrate, it was desirable
to have the lower lid in control of eye closure. Only in those forms in
which, by and large, the eyes are carried higher (crocodiles, some birds,
nearly all mammals) does the upper lid become the more active of the
two. In very small mammals (e.g., the house mouse) the lower lid may
move more than the upper, as in the creepers and crawlers of the lower
classes.

The horizontal orientation of the palpebral fissure has had at least
two effects upon the structure of the eyeball itself. It has allowed the
development of 'ellipticity', of horizontally extended corneas and pupils,
in those mammals which have great need of a wide visual field. It
accounts also for the well-nigh universally vertical orientation of slit
pupils in terrestrial forms. In bright light the lids, partially closed as we
so often see them in a basking cat, are not unimportant in aiding the
pupil to control intra-ocular illumination — as witness the fact that where
the slit pupil can be entirely closed, it is most often in forms which lack
mobile lids (see Chapter 9, section C). Where the slit pupil is vertical,
the squinting of the lid opening at right angles to the slit makes of it a
better stenopaic aperture, combatting the optical imperfections of the
peripheries of lens and cornea, yet still admitting enough light because
of the great retinal sensitivity of slit-pupilled eyes. It seems significant
that the vertical orientation of the slit pupil was not finally adopted until
the vertebrates came on land and developed lids (Table VI, pp. 220-1).

Peculiar Status of the Elasmobranchs — Our whole philosophy of
the basis of the contrast between the fish eye (with its lack of a ciliary
corona, lids, and glands, and its spherical lens in contact with a flat cor-
nea in a shallow globe) and the typical 'air' eye (in which ciliary folds
are present, the lens flattened and drawn back from an arched cornea
kept moist by glands and the lids which spread their products) is rather
rudely disturbed by the elasmobranchs. In some of these fishes all of the

ESSENTIAL PROBLEM IN AMPHIBIOUS VISION 429

above, 'terrestrial' characteristics are present along with others such as
the salamander-like accommodation; and most of them occur in any
given species of the group. If it were not almost unthinkable, we might
conclude, from a cursory examination of a shark eye, that the elasmo-
branchs must once have lived on land and^ like the whales, secondarily
returned to the ocean! Surely, these peculiarities of the elasmobranch eye
ail have explanations other than those which hold for their seeming
counterparts in the higher vertebrates; but we cannot be sure at present
that we know quite all the answers.

The arching of the elasmobranch cornea and its distance from the lens
appear to go simply with the method of accommodation peculiar to the
group (see p. 260) . The ciliary and iridic folds are probably mechanical
devices for anchoring the thick zonule (whose rim covers the whole sur-
face of the ciliary body), and not secretory — indeed, there is reason to
suspect them of being absorptive. But the presence of distinct upper and
lower lids in so many forms, the lower lid often having an extra trans-
parent fold comparable to a frog's 'nictitans' (Fig. 131b, p. 382), is a
deep mystery. The complex is best developed in the largely bottom-
loving sharks (galeorhinid) which, if they were teleosts, might be expected
to show the simpler protective device represented by the secondary spec-
tacle. The great blue shark Prionace glauca, a pelagic species which is
most active at night (when it hunts by scent) has been observed to blink
the nictitans rapidly in bright light when pursuing prey or when other-
wise excited, as though the irritation of the light were controlled some-
what by the membrane. But there is no evidence that this is always, or
ever, its primary purpose. Indeed, Franz found that Scylliorhinus and
Mustelus would not use their lids to shield their eyes from the strongest
light, though they would struggle violently to get away from it; nor
would Ra]a, capable of concealing the eye by retracting it, do so in order
to avoid dazzlement.

An interesting problem awaits the investigator who attempts to corre-
late the palpebral complex of the elasmobranchs with something else in
their biology. Its solution will be most welcome.

(C) AiR-AND- Water Vision

The Main Problem — Those vertebrates which wish to eat their cake
and have it too, by attempting amphibious vision, have a considerable
problem. If they happen to be fishes, they not only have their optical
difficulties in seeing in air, but must somehow get along without the

430 ADAPTATIONS TO MEDIA AND SUBSTRATES

elaborate adnexal pattern which terrestrial animals have found essential.
If they happen to belong to the great sauropsidan-mammalian majority
of air-and-water lookers they have no worries on this latter score; for
though their lids and glands are not needed under water, neither are
they any great handicap. But these secondarily aquatic forms which still
cling to the land for feeding and breeding purposes have to compensate
somehow for the optical loss of the cornea, when this important refrac-
tive structure is 'gone with the water'.

In attempting to combine two very diverse optical arrangements within
one visual organ, amphibious vertebrates are in a position analogous to
that of the twenty-four-hour animal with respect to the extremes of
illumination. The arhythmic animal, be it remembered, must effect a
mixture of compatible adaptations to both bright and dim light. If in-
stead he merely 'strikes an average', he ends up not by being arhythmic
and maximally independent of the rotation of the earth, but crepuscular
and restricted more than ever in his hours of activity. Striking an average
in the eye for both air and water is well enough as far as the adnexa are
concerned. We see just such a situation in the Amphibia, whose half-way-
evolved lids and glands allow them freedom in the air, provided that the
air be humid. But half-way adaptation of the eyeball itself is impossible —
there is no visual medium intermediate between water and air. However
moist the atmosphere may be, seeing through it demands strictly aerial
optics — and seeing through water demands, just as sternly, aquatic optics.

The problem boils down essentially to the production of an exceptional
range of accommodation — sufficient, in an amphibious fish, to overcome
the increased myopia which appears in the eye in air; or sufficient, in a
higher vertebrate, to neutralize the hypermetropia which instantly super-
venes when the cornea is immersed in water. These added demands upon
the accommodation of a given amphibious animal could never be met by
the mechanism characteristic of his immediate one-medium relatives, and
are usually countered by supplementary devices which increase the defor-
mation of the lens at a considerable cost in muscular effort. A very few
vertebrates, however, have found easier ways of producing interchange-
able aerial and aquatic systems of optics without becoming intra-ocularly
muscle-bound. They meet the problem with a bare minimum of muscular
exertion within the eyeball, or even with none whatever — just as a few
vertebrates restricted to either aquatic or aerial vision have been clever
enough to obtain good images over a range of distances without the use
of dynamic accommodation at all (see pp. 254-7) .

AMPHIBIOUS VISION IN TELEOSTS

431

Amphibious Vision in Teleosts — It is only among the teleosts that
we find fishes which spend enough time out of water to have any possible
use for air-and-water vision. The number of such teleosts is surprisingly
large. To mention the best known cases, there are the true flyingfishes
(but not the 'flying' gurnards) , the imitative hatchet-fishes {Gasteropele-
cus, Thoracochdrax, et al), and the butterfly-fish or 'freshwater flying-
fish', Pantodon. These forms come out of water for an appreciable frac-
tion of a minute at a time — ^up to 40 seconds, in flyingfishes — though
they are not amphibious inasmuch as they never come on land, or on

J^

\

Fig. 145 — Periophthalmus koelreuteri.

a, entire animal, x 'A. After Hess, b, eye in vertical sertion. From Franz, after Karsten.
c- primitive cornea; /- anchorage of suspensory ligament of lens; /- secondary speaacle.
c, d, e, positions assumed by the eyes of Periophthalmus, Boleophthatmus, et al, showing
alteration of visual lines and formation of transitory lower lids. Redrawn from Hein.

board ship, except as a fatal accident. Nothing much is known about the
eyes of any of them. Then, there are such fishes as the 'climbing perch',
Anabas, which emerge onto land for periods limited by the considerable
oxygen content of their labyrinthine water reservoirs; and some blennies
which perch on rocks for long periods with the tail kept in the water for
respiratory purposes. Again, the eyes of these fishes are largely unstudied,
though Anabas is known to be emmetropic in water and to have no
accommodation — hence, a forbidding degree of myopia in air, with the
eye probably almost useless in that medium except for brightness- and
shadow-perception.

432 ADAPTATIONS TO MEDIA AND SUBSTRATES

The most nearly terrestrial of fishes are certain gobies and blennies.
Among the gobies, ecologically speaking, almost anything may happen.
They present a wide variety of bizarre adaptations and hold a number of
records of various sorts. Some of them, less than half an inch long when
fully grown, are the smallest of all vertebrates. Others, Periophthalmus,
Boleophthalmus, et al, actually prefer to spend most of their time out of
water on a mud-flat exposed at low tide. Most gobies have the pelvic fins
converted into an adhesive disc, and some of them cling with this to
wave-dashed rocks or to the sides of burrows, like the blind Typhlogobius
mentioned above (p. 388). It is not surprising that some surf -tossed gobies
have sought still greater security by getting out of the water altogether.
A still larger number of the blennies inhabit rocky places between the
tide-marks. The blennies lack the suctorial attachment organ, but their
amphibious members equal the amphibious gobies in pertness, fearless-
ness, and lizard-like agility. In keeping with these qualities they have
speedier accommodation than any other fishes.

Periophthalmus and its relative Boleophthalmus, among the mud-skip-
pers of the coasts of Asia, West Africa, and Polynesia, have had a good
deal of attention. Their eyes are set in high turrets (Fig. 145a) and are
practically on universal joints, compensating thus for the lack of a neck
which becomes quite a handicap on land. They rotate under secondary
spectacles which appear to be their only protection against desiccation.
When deeply retracted into the head for mechanical protection, the eyes
are covered by puckered skin-folds somewhat as in the rays, anglers, and
turret-eyed flatfishes, which similarly have the body often in one medium
(sand) while the eyes are out in another (water). When the eye of a
mud-skipper is turned downward for horizontal vision like that of other
fishes, the skin forms a sort of lower 'lid'. This lid is only temporary,
and is abolished when the eye is elevated. The manner in which the infer-
ior rectus and inferior oblique muscles are crossed, in the mud-skippers,
makes of them a sort of cat's-cradle which raises the eye in its conning
tower. There is thus no need of a special levator bulbi muscle such as the
frog possesses.

In an average adult of Periophthalmus koelreuteri, the eyeball is 4.0
mm. in diameter with a very large (3.8 mm.) and strongly curved cornea
(Fig. 145b). The lens is slightly flattened, its equatorial diameter being
1.14 times the axial. The static optics of the eye are thus those of a land
animal: Periophthalmus, when in the air, appears to be emmetropic or
even slightly hypermetropic — but the fish is then actually accommodating

AMPHIBIOUS VISION IN TELEOSTS

433

maximally. When it goes under water the accommodated eye naturally
becomes strongly hypermetropic. Whether perfect emmetropia can be
restored in water by complete relaxation of the retractor lentis is un-
known, and unlikely. The great increase in the brightness of the retinal
image in air is reflected in a predominance of cones, and their distri-
bution is clearly adaptive to the downward incidence of the sunlight. A
substantial portion of the inferior half of the retina is pure-cone, the
remainder duplex (with about 80% cones) except for a narrow pure-rod
zone in the extreme superior periphery. The pigment epithelium is excep-
tionally thick, and rich in pigment. The rich cone population frees the
animal from dazzlement, and makes possible a visual acuity adequate to
the pursuit of its active food (largely insects) in a quite lizard-like
fashion, the fish skipping about upon its stiff pectoral fins. By compari-

Fig. 146 — Dialommus juscus, an amphibious blenny. Based upon figures of Breder and Gresser.

a, anterior end. b, schematic front view of eye. c, schematic horizontal section of eyeball.

c- cornea; i- iris; /- lens; w, w- unpigmented 'windows' in cornea.

son with even so sharp-sighted a predator as the pike, Periophthalmus
shows to advantage; for it has been found to have about 225,000 visual
cells and 90,000 ganglion cells per square millimeter of retina, while
counts in Esox have shown 50,600 rods, 5600 cones, and 3512 ganglion
cells per square millimeter.

One of the surf-loving rock blennies, Dialommus juscus, has been
recently studied, though the investigators had to give up when they tried
to interpret the eye. At first glance, Dialommus appears to have two
pupils, fore and aft (Fig. 146). There is actually but one aperture in the
iris itself, the two clear areas being in the cornea (Fig. 146c) which is
otherwise heavily pigmented — a great exaggeration of the eyeshade-like
dark pigmentation of the upper part of the cornea in some of the needle-
fishes and in Torpedo. Nothing is known of the refraction and accommo-
dation of Dialommus, but it seems to have made an ingenious adjustment

434

ADAPTATIONS TO MEDIA AND SUBSTRATES

to the greatly augmented illumination of the eye when it is in the air.
Since the lens prevents the pupil from closing, the effective aperture of
the eye has had to be cut down, and this has been done without sacrific-
ing periscopy in the all-important horizontal plane. The total area of the
two corneal windows is no greater than that which a single, central win-
dow would have if its diameter were equal to 1.414 (^V^ ) times that
of one of the two little ones. But such a window would limit the visual
field disastrously, particularly considering the bothersome absence of a
neck. If this interpretation is correct, we must suppose that Dialommus
does not have as insensitive (cone-rich) a retina as Periophthalmus, else
it would not need its blacked-out cornea; but no well-preserved material,
in which the retina could be studied, has become available.

Fig. 147 — Anableps anableps, the 'four-eyed fish'. From Walls.

a, schematic vertical section of eye. After Piitter. S,S- plane of water surface; A- line of
sight upward into air; W- line of sight downward into water, b, pupil of 35mm. larva,
with division commencing, c, pupil of adult, completely divided. After Schneider and
von Orelli. /-iris; p- pupil; y- sclera. (See frontispiece).

Another fish — a cyprinodont this time — really does have two pupils
(Fig. 147). This is the famous 'Cuatro Ojos' or four-eyed fish of north-
ern South America and western Central America, Anableps (see frontis-
piece) . The eyes are similar in the three species of this genus. The upper
pupil is the larger of the two and is normally out of water; for the animal
is a top-minnow, and swims sedately at the surface in quiet waters. The
eye is elevated just enough in the head so that the water-line cuts it neatly
in two. There are no devices to guard the upper half of the cornea against
drying, so the fish periodically 'dunks' it.

Internally, the Anableps eye combines an aquatic optical system har-
moniously with an aerial one, in a perfectly static situation (Fig. 147a).
The lens is pyriform, and an imaginary extension of its long axis would
pass through the superior retina and through the inferior pupil. The cur-

AMPHIBIOUS VISION IN TELEOSTS 435

vatures of the lens which are used in looking through the lower pupil,
into the water, are thus sharper than those aligned with the inferior retina
and the superior pupil. But the inferior retina looks up through the optic-
ally effective corneal surface which is exposed to the air. Aerial and
aquatic objects are thus focused simultaneously on separate regions of
the retina. It is perhaps significant, in view of the impossibility of effective
osmosis over a half-submerged cornea, that Anableps is one of the two
or three teleosts known to have ciliary folds. At any rate, the eye of the
Cuatro Ojos is one of the most remarkable of vertebrate eyes. The reader
has probably by now given up trying to select the most remarkable!

Apart from the species of Anableps, there are other teleosts which
never leave the water except in an occasional leap, but give a great deal
of attention to out-of -water objects. The trout, for example, certainly sees
flies before they hit the water and does not always wait for them to do
so. The wise dry-fly angler arouses the trout's interest by making 'false
casts', in which the fly is not allowed to touch the surface. But the trout
is a piker compared with a certain very famous looker-out-of -water. This
is the archer-fish, Toxotes jaculator, which spits a slender stream of water
at an overhead insect with excellent aim, knocking it down to the sur-
face-film of the water, from which it cannot escape. Toxotes is not
described as ever putting its eyes out of water, and should therefore
exhibit no adaptations for amphibious vision. But if the hydraulic artil-
lery of the archer-fish is dependent upon what he can see through the
surface from below, he must have a truly remarkable trigonometric range-
finder in his brain to cope with the ever-varying distortion of angles,
sizes, and distances (see pp. 377-9). Moreover, Toxotes does not, like
Anableps, have the benefit of the glassy calm of freshwater lagoons; but
the species does live in fairly calm brackish estuaries.

One of the Indian mullets, Mtigil corsula, presents an interesting habit.
This fish swims in small schools, in quiet waters. The protruding eyes
are set high upon the sides of the head and are very mobile — especially
antero-posteriorly. They are sometimes converged forward. The mouth
is ventral, and the fish feeds upon filamentous alga and upon caddis-
flies trapped in the surface film. As the fish cruises along with the gape
at the surface, the eyes are well out of water. The vision in air appears
to be excellent, and the eyes, with a lens diameter-thickness ratio of 1.17
(compare Periophthalmiis, 1.14) are definitely adapted for aerial vision.
It has been suggested that this use of the eyes has been 'caused' (allowed,
rather!) by the underslung mouth — present in the mud-skippers too, and

436 ADAPTATIONS TO MEDIA AND SUBSTRATES

perhaps there also a predisposing factor in the raising of the eyes. On
the other hand Anableps, being a top-minnow with a terminal mouth to
begin with, has never needed to raise its eyes completely out of water in
order to feed from the surface film. Like Anableps, Mugil corsula peri-
odically dips its head under water to moisten the cornea.

Amphibians and Crocodilians — Probably none of the Amphibia or
Crocodilini are capable of air-and-water vision. In both groups the eyes
are raised in the head so that they, and the nostrils, can be in air while
the rest of the body floats awash in concealment from enemies and prey.
The implication is that the eyes are adjusted primarily for aerial vision
and are of little or no use under water; and what little information we
have bears this out. In amphibious and terrestrial amphibians the eye
takes on its aerial adjustments during metamorphosis: the lids develop,
the primary spectacle becomes a part of the cornea, and the latter be-
comes arched, while the lens departs to some extent from the perfectly
spherical form which it has in the aquatic tadpole. The refractive index
of the lens remains fairly high, however, with a value of 1.44-1.45 in
common frogs. These animals are emmetropic in air, but have insufficient
accommodation to be anything but strongly hypermetropic in water.
Though the ranid frogs are the most amphibious of amphibians, they
have less accommodation than the strictly terrestrial bufonid toads,
which may have as much as five diopters. Some tree-frogs, just as ter-
restrial as the toads, may however have none at all.

Whether the crocodilians are emmetropic in either air or water is not
known, but they have so little accommodation that they could not pos-
sibly have clear vision through both media. Their nocturnality and crude
central images make this deficiency of no consequence to them. Spend-
ing much time basking out of water in dry, sunlit places, the crocodilians
have much more perfectly 'terrestrial' adnexa than do the Amphibia.

Turtles — With the turtles, we come to the first group of amphibious
vertebrates in which we can be sure that a perfect focus is attainable
whether the head is immersed or above the water surface. They supple-
ment the already superb sauropsidan machinery of accommodation (see
pp. 269-79) with the powerful sphincter iridis muscle, which squeezes the
front of the lens (Fig. 148) into a curvature of very short radius — a regu-
lar 'anterior lenticonus'. The range of accommodation is thus very great,
easily sufficient to cancel the loss of the corneal surface. The deformation
of the lens is facilitated by its extreme softness, which is maximal for all

AMPHIBIANS, CROCODILIANS, TURTLES

vertebrates and exceeds that of even the lizards, whose fresh lenses will
drool through one's fingers if one attempts to hold them in the hand. As
might be expected, the range of accommodation is rather less in the com-
pletely terrestrial tortoises and in the thoroughly aquatic sea turtles than
it is in the in-and-out pond-dwelling majority. In Emys, a pond genus,
for example, the ciliary processes bear on the lens (Fig. 110, p. 277), and
during accommodation the lens is squeezed equatorially, its diameter
reduced. In the terrestrial Testudo, the ciliary processes touch the lens
but the deformation of the latter in accommodation is much less than in
Emys, and its diameter is not affected. In the marine Thalassochelys, the
ciliary processes do not reach the lens, which is relatively small and is
much more nearly spherical than that of other turtles. Konig found a
transversalis muscle (p. 269) in Emys and Thalassochelys, but not in
Testudo, whose embryonic fissure is entirely closed.

I

Fig. 148 — Accommodation in turtles.

a, b, relaxed and accommodated conditions in Emys orbicularis. x4/4. From Franz, after
Beer, c, diagram showing roles of sphincter iridis and ciliary muscles in produrtion of
anterior lenticonus. c- ciliary muscle; s- sphinrter iridis muscle; o- scleral ossicle.

The female marine turtle is in a bad way visually when she comes
ashore at night to lay her eggs, for her aerial vision must be hazy and
dim even if the moon is bright; and though she closes her eyes tightly
when digging her nest, the reduced lids are inadequate to prevent the
eyes' getting clogged with sand. All in all, she must be very glad to get
back in the water, toward morning!

Since the lens of a turtle always projects through the pupil, to let the
iris get a grip on it during accommodation (Fig. 148c), the pupil can
actually close but little if at all. But the turtles have obtained immunity
from dazzlement by eliminating nearly all of their rods, though they
might perhaps have kept a well-balanced duplex retina if they had also
retained efficient photomechanical changes. They are thus under some
handicap in seeing under dim underwater conditions, and undoubtedly
such bottom forms as the snappers and musk-turtles hunt chiefly by

438 ADAPTATIONS TO MEDIA AND SUBSTRATES

touch and smell. It is perhaps because of this handicap in sensitivity that
the turtles have developed the most completely transparent corneae,
humors, and lenses of any vertebrates.

Amphibious Squamates — Among the lizards there is at least one
conspicuously amphibious form, the marine iguana of the Galapagos
Islands, Amblyrhynchus cristatus. These great lizards feed mostly upon
bottom sea-weeds at some distance from shore; but it was Charles Dar-
win who first demonstrated that their every instinct is to cling to the
land or make for shore when they are attacked or frightened. It is be-
lieved that they feed in the sea out of dire necessity rather than choice.
Their eyes have never been studied, but it is unlikely that they are any-
thing but aerial in their adaptations. It will be recalled that the very
thoroughly aquatic sirenians, with similar feeding habits, get along with
eyes which can only be very poor-sighted under water.

There are many amphibious snakes. The most completely aquatic of
them, the marine cobras (Hydrophiinae) and the fluviatile Homa-
lopsinas, are practically unknown, ophthalmologically. The river snakes
—Acrochordus javanicus for example — have the eyes toward the top of
the head, but this does not necessarily mean that they are ever used out
of water any more than does the same situation in the angler-fishes and
star-gazers.

Years ago, Beer studied Natrix tessellatus, a European relative of our
common water snakes, and found it to differ in two respects from ter-
restrial colubrids. The lens was not completely firm, and when removed
from the eye it took on the shape it has in accommodation, just as does
a human lens. This unusual softness permits the tessellatus lens (and
those of our Natrix species, rainbow snakes, etc.?) to be squeezed by the
pupillary sphincter as in the turtles, thus greatly extending the range of
accommodation. In other snakes it is only those circular muscle fibers
massed toward the root of the iris which are much concerned with accom-
modation, and the process (see p. 282) changes only the position of the
lens and not its form. The sea-snakes contract their pupils to stenopaic
pinholes when out of water, thus solving their problem somewhat as the
seals (v. i.) have done.

Amphibious Birds — The birds had no sooner come into existence as a
group than some of them, like the extinct Hesperornis, promptly took to
the water. Many groups, and many scattered species, have become more
or less aquatic since. Some are very decidedly so, and can fly as well (or

AMPHIBIOUS LIZARDS. SNAKES, BIRDS 439

better) under water as in the air — such birds as the loons, grebes, snake-
birds, auks, and penguins, all of which pursue and catch fishes. The
penguins cannot fly in the air at all; and most of us have seen how much
of a chore it is for a loon to 'take off'. The cormorants are also speedy
fish-chasers, though they perhaps use their feet more than their wings.
Still other birds swim on the surface, and up-end to feed on plants or
fishes in the water beneath: ducks, coots, mergansers, etc. A host of
birds, most of which can swim on the surface to rest and sometimes dive
from the surface, have the habit of flying over water and plunging into
it momentarily to grasp a finny prey : pelicans, gulls, terns, shearwaters,
petrels, gannets, boobies, albatrosses, ospreys, sea-eagles and so on —
and one of the cormorants, the Peruvian guano-bird.

Three kinds of birds have particularly unusual water-habits — the tor-
rent ducks, the dippers, and the kingfishers. The kingfishers may plunge
from the wing, but more commonly do so from a perch, and thus come
between the flying fishers and the tall waders like the herons, whose
perches are their own long legs. Their eyes, as we shall see shortly, are
a little reminiscent of those of Anableps. The dippers are an especial
phenomenon, for though no birds are so thoroughly wedded to water
(they will not even fly over dry land!) they are regarded by ornitholo-
gists as having no adaptations whatever for water. The dipper or water-
ouzel is simply a thrush which walks and flies unconcernedly under water
to find his insect food, holding himself down when necessary by grasping
stones with his feet, which even lack the ubiquitous webs of other water
birds. His eyes have never been studied, but will almost certainly prove
to have amphibious adaptations even though such are lacking every-
where else in the body.

In general, the eyes of all of these birds are built primarily for aerial
vision. The extent to which water birds have attained underwater seeing-
ability goes largely with the duration of their underwater periods, and
hence, naturally, with their general bodily modification for submerged
activity. Thus, the penguins head the list with eyes which are entirely
devoted to water vision, with highly responsive pupils and with no special
range of accommodation or other device to make them very useful in
air, in which they are notoriously myopic. It has often been pointed out
that a swimming penguin is quite dolphin-like in its streamlined form,
with even the same color-pattern — black above and white below. Pen-
guins are so completely adapted to water that they have hair-like feathers
in enormous numbers, a whale-like blubber for heat insulation, and are

440 ADAPTATIONS TO MEDIA AND SUBSTRATES

believed by non-scientific (and some scientific) observers to have their
habit of eating pebbles for the purpose of ballasting, as in the case also
of the elephant seal. They feed largely upon the same squids and 'krill'
as do the baleen whales, but catch them individually and visually, rather
than by trawling, for which they have no equipment.

Next come the cormorants, loons, auks, sea-ducks and diving ducks
in general. All of these are able to secure sharply-focused images in both
air and water, though not all by the same means. Last come the many
species of plungers exemplified by the terns. These probably have no
special ability to see in water, and characteristically make only a blind
stab for the fish which they have spotted from the air. They often miss,
as compared with the birds which beat the fishes at their own game of
underwater swimming.

The ocular devices employed by the birds with truly amphibious vision
fall into three categories, exemplified respectively by the cormorants, the
diving ducks, and the kingfishers. The simplest of these devices is that
of the cormorant, and is developed to about the same degree also in the
booby :

The cormorant compensates for the loss of the cornea in exactly the
same way as does the turtle. Its iris is the most muscular one in all the
vertebrates, and the deformation of the lens by the powerful sphincter
is extreme (Fig. 149). During the process, the pupil at first closes slightly,
but then enlarges again as the iris tissue is rolled outward by its pressure
against the lens. The lens is as soft as that of a turtle, which probably
cannot be said of that of any other bird. In contrast to the few diopters
of accommodation of land birds, the cormorant has 40-50 diopters — two
or three times the range of the human infant, which is the most accom-
modating (?) of mammals, but owes its extensive range to the juvenile
pliability of the lens and not to any real need.

The diving ducks, loons, and auks have much more powerful iridic
sphincters than do the non-diving ducks and land birds. They have an
action approaching that in the cormorants, whereas in other birds the
iris molds the lens only passively as the lens is pressed against it by the
ciliary processes. But these birds are as well off under water as the cor-
morant, and at less expense of muscular energy. Ischreyt, the leading
student of their eyes, found that in all of them the nictitating membrane
has a clear, lens-like central window, composed of highly refractive ma-
terial which is capable of bending light rays even under water. If we
compare the devices of Anableps and the kingfishers (r. i.) with bifocal

AMPHIBIOUS BIRDS 441

spectacles, we may compare that of the sea-duck with a 'contact lens'!
Captive American mergansers have been observed to pursue their trout
and salmon prey by sight. They can evidently accommodate sufficiently
under water to give themselves a near point within ten feet, for they
unerringly follow the movements of their victims at that distance.

The size of the cornea has been reduced by the conversion of a zone
of its substance, near the limbus, into opaque sclera-like material. In the
cormorant a further similarity to some aquatic mammals is seen in the
thickening of the sclera at the sclerocorneal junction. In all of these birds
the scleral ossicles are particularly heavy, so thick as to have marrow
cavities within them like those of the hawks (Fig. 112, p. 280) ; and div-
ing ducks have thick corneas. These thickenings possibly stiffen the wall
of the eyeball against the shock of immersion, perhaps only support it

Fig. 149 — Accommodation in amphibious birds.

a, anterior segment of cormorant, Phalacrocorax sp., in relaxation. Redrawn, modified, from
von Hess, b, same as a, in accommodation, showing action of the powerful iris sphincter.
Note that th« fibers of the pectinate ligament are taut and that the spaces of Fontana,
behind them, have become dilated by the pull of the iris.

cp- ciliary process; is- iris sphincter; pi- pectinate ligament; so- scleral ossicle.

against the unusual pull of the augmented accommodatory apparatus.
One part of the latter is at a low ebb in these underwater swimmers :
/. e., Crampton's muscle. Its function being chiefly to shorten the radius
of curvature of the cornea as an aid to accommodation for near objects
(p. 281), and there being no point to any manipulation of a refractive
surface which is just 'not there' under water, this muscle is reduced in
some amphibious species and is absent in others. There is none in the
cormorants, it may be lacking or small in loons and auks, and it is small
in the diving fuliguline ducks (as compared with the non-diving anatine
ones). On the other hand the muscle of Briicke (Fig. 112) is massive in
cormorants, stronger in diving than in non-diving ducks; and in cormo-
rants and in the gannet (Morus bassana) it is most exceptional in con-
taining circular fibers like those of the human muscle of Miiller.

442 ADAPTATIONS TO MEDIA AND SUBSTRATES

The kingfishers — if our interpretation of their eyes is correct — are
quite alone among birds in having clear vision through both air and
water without need of accommodating at all as they pass from one
medium into the other. In the European Alcedo a. at this, at least,
Kolmer found the following situation :

The axis of the eye is somewhat shorter than its equatorial diameter.
Near the ora terminalis, temporally, there is a second fovea which is as
well-developed as the central one, and which sits in an outpocketing of
the eyeball wall. The body of the lens is nearly symmetrical, but the lens
as a whole, due to variation in the thickness of the annular pad, is
strongly egg-shaped with its narrow end aimed toward the temporal
fovea. The long axis of the lens is thus parallel to the palpebral fissure.
The ciliary body is also strongly asymmetrical, narrowed nasally, and
has particularly powerful processes around the narrow end of the oval
lens. There is a well-developed sphincter iridis, but otherwise the iris and
ciliary body are actually poor in muscle elements; and the chorioidal
muscle-cells, said to be common in the neighborhood of the fovea cen-
tralis in other birds (see p. 281), are lacking. Kolmer 's interpretation fol-
lows— how right it is, we cannot be sure at present; perhaps the investi-
gator has been more ingenious than the bird itself :

As the kingfisher descends through the air, the prospective prey is
kept in sharp focus on the central fovea of one eye, and the other eye
progressively converges in sympathy. The lens is moved nasally as well
as squeezed, due to the asymmetry of the ciliary body. This, together
with the evaginated location of the temporal fovea, puts the latter so far
from the optical center that its line of sight — not in use in air — is ex-
tremely myopic. As the bird enters the water, the cornea 'disappears'
and at once the prey is sharply registered on the temporal foveae of both
eyes and thus is seen binocularly. At the same instant, the line of sight
of each central fovea becomes hopelessly hypermetropic and remains so
until the bird emerges into the air once more. The kingfisher seems to
have improved on Anableps, in devising a lazy way of accomplishing an
end which costs the turtle or the cormorant many a calorie.

Amphibious Mammals — The statement is often made that there is
no mammal which cannot swim if tossed into water. There are a great
many species which do not have to be thrown in. Brazier Howell, in his
work on aquatic mammals, mentions about three score which he terms
definitely (though not obliged to be) aquatic in their predilections.

AMPHIBIOUS MAMMALS 443

These are nearly all placental mammals — there are but one aquatic mon-
otreme (Ornithorhynchus) and one aquatic marsupial, the water opos-
sum iChironectes).

Of those which are amphibious — that is, excluding the whales and sea-
cows — the vast majority on Howell's list are small members of the In-
sectivora and Rodentia. Howell believes that these, and the platypus,
probably keep their eyes closed when submerged. The white bear and
several mustelid carnivores are piscivorous and must use their eyes under
water, but only for the European otter (Lutra vulgaris) have the eyes
been described in any detail. The only other amphibious mammals whose
eyes have had any great attention are the beaver, the hippopotamus, and
particularly the Pinnipedia — seals, sea-lions, and walruses. We will con-
sider these types in the order of their perfection of visual air-and-water
adaptation :

The hippopotamus stands at the bottom of the list. From the situation
in the frog and the alligator, we should at once become suspicious upon
noting that the hippo's eyes are elevated like his nostrils, and may thus
be kept in the air while the rest of the body is submerged. This is an
aquatic adapation right enough, but it is definitely not an adaptation to
aquatic vision. The adnexa have become modified, though not nearly as
much as in the sea-cows. The lids form a ring bearing only traces of
lashes, and close as the eye retracts. The nictitans is reduced and can
cover only half of the cornea. The nasolacrimal duct has disappeared.
No known aquatic or amphibious modifications occur in the eyeball it-
self. The hippo is unique in that it spends most of its time in the water,
but does all of its feeding on land. In keeping with these habits, the pupil
is horizontal like that of terrestrial ungulates, to extend the visual field
somewhat in the plane in which the animal needs most of its wariness.
The raising of the orbits clearly represents a device for keeping the eyes
in their only appropriate medium for as much of the time as possible.

Studies on the eye of the Canadian beaver are not yet complete. The
animal is essentially diurnal when quite unmolested, but does not have
the yellow lens (see p. 204) characteristic of other diurnal rodents.
Though the eyes are stated by Howell to be the most dorsally-directed
among all rodents, the orbits form no turrets as in the hippopotamus.
There is thus no a priori reason to suppose that the beaver cannot see in
the reduced light under water. The European beaver is stated to have a
cornea much thicker than the sclera, which perhaps helps the eyeball to
withstand the impact on the water surface, in diving. The ciliary body

444 ADAPTATIONS TO MEDIA AND SUBSTRATES

is greatly developed, and further studies may complete a picture of equal
visual capacity in the two media, in each of which the beaver certainly
performs as though it had excellent vision.

The otter has repeated the device of the turtles and the cormorants.
The ciliary muscle is very well developed, and in addition there is an
enormous sphincter in the iris which squeezes the anterior portion of the
lens. The range of accommodation is unknown, but in air the eye is
emmetropic or slightly hypermetropic, and the otter is known to hunt
under water largely by sight despite the small size of the eye. It is entirely
likely that the focusing power of the cornea is not at all missed. The
adnexa of the otter appear to be quite unmodified. The nasolacrimal
duct is nowadays stated to be present, though this was once denied.

The Pinnipedia, first cousins of the terrestrial carnivores, are more at
home in the water than any other mammals except the whales. As with
the whales, there are two large divisions of the group which differ some-
what in the character of their adaptations. The Phocidse or 'true' seals
are extremely clumsy on land owing to the profound modification of
their limbs; and they have larger eyes in keeping with their habit of feed-
ing upon relatively small prey caught in comparatively deep water. The
elephant seal feeds at depths of three hundred to seven hundred feet.
The Otariidse (sea-lions or eared seals) are more comfortable on land,
being still able to turn their hind feet into something like the standard
mammalian walking position. They feed on fairly sizable squids and
fishes, and are not believed to swim very deeply. Intermediate between
these two families in many structural respects come the moUuscivorous
Odobaenidae, the walruses.

The visual axes of pinnipeds are canted upward to some extent rather
than downward as in the strictly water-seeing cetaceans. This is prob-
ably related to their vital need of spying out the landing place before
crawling out onto it — their terrestrial clumsiness is considerable of a
hostage to fortune in the form of the nearest white bear. The eyes aim
strongly laterally, the binocular field being about as wide as in the aver-
age terrestrial carnivore. In the elephant seal, the young animal has
strongly frontal eyes which swing farther laterally during growth — the
reverse of the usual ontogenetic change in the attitude of the optic axes.
The lid opening is shorter than the diameter of the cornea, which com-
pared with that of a fish is relatively small to begin with. But this is no
sign of degeneracy — the seals roll and wriggle so much, in their acrobatic
swimming, that they would probably be hard to approach unseen even if

AMPHIBIOUS MAMMALS 445

they had tube vision, and lacked what little eye mobility they do have.
The lids are closed by an orbicularis oculi, and there is a weakly devel-
oped tarsus in the upper lid only, with no Meibomian glands. The
corneal epithelium is strongly keratinized, and in addition an abundance
of protective oil is produced by the Harderian gland, which is very large,
the lacrimal being only one-fourth as large (though in the fetus it is tem-
porarily the larger of the two — ontogeny bearing out the probable course
of phylogeny). Associated with the Harderian gland there is a fully-
formed nictitans containing a stiffening cartilage. There is no trace of a
nasolacrimal duct, even in the embryo, and the gummy tears are con-
stantly in evidence when the animal is on land.

The eyeball is large in absolute size as well as relative to the body. In
the common 'trained seal' or California sea-lion (Eumetopias californ-
icus) it is 39 mm. in diameter both horizontally and vertically, the axis
showing some shortening (to 35 mm.) in keeping with the fish-like optics
of the eye. The axis in seals varies between 81% and 91% of the vertical
globar diameter. In a half grown (ten-foot) elephant seal (Macrorhinus)
the globe was found to be 63.2 mm. in horizontal, 65.7 mm. in vertical
diameter, with a 55.7 mm. axis — thus, average with respect to the rule
just stated, but constituting one of the rare examples of vertical ellip-
soidality among vertebrate eyeballs. The eye of the little Phoca vitulina
or harbor seal is a bit larger than our own, with the horizontal and verti-
cal diameters equal, as is the rule in the group.

The cornea is circular or slightly elliptical horizontally, and is only
slightly arched (except in Macrorhinus) over an anterior chamber which
is quite un-fishlike in depth (Fig. 150), periscopy being obtained dynam-
ically rather than statically, as mentioned above. In Eumetopias the
cornea measures 30 by 25 mm. and its arch is 6.5 mm. high. The pinniped
sclera is thickened a bit in the fundus, and the optic nerve sheath is
heavy; but these structures are not all out of proportion to the internal
ocular volume as they are in the much larger eyes of the whales. The
chorioid is orthodox except for the great area and great number of
lamellae of the tapetum cellulosum. The ciliary body is very firmly fused
to the sclera so that the chorioid cannot be pulled upon during the strong
accommodation. It has circular muscle fibers as well as long, powerful
meridional bundles, and bears moderately long processes which usually
just reach the lens.

The lens is spherical in Phoca, and it never has the equatorial diameter
more than 1.14 times the axial. It is proportionately much larger than in

446

ADAPTATIONS TO MEDIA AND SUBSTRATES

sirenians and whales, but it is not 'nocturnal' in size. In fact, it has about
the same relative diameter equatorially as that of man, being 37% of the
vertical diameter of the eyeball in Phoca vitulina and 38.5% in Eumeto-
pias. These ratios are quite distant from those obtaining in nocturnal
carnivores (about 50%) and are closer to those in the twenty-four-hour
ungulates (around 40%) . The lens being spherical, it can be thought of
as being greatly thickened; but this is an adaptation to the 'loss' of the
cornea in aquatic vision, and not to nocturnality; for, the seals are diur-
nal. Its refractive index, like its shape, is on a par with that of fishes, and
Matthiessen's ratio (p. 264) probably holds for its relationship to the
retina. In consequence of the sphericity, the border of the lens epithelium
reaches around past the equator of the lens onto its posterior face, as it
does in fishes, aquatic amphibians and tadpoles, and toothed whales.

cornea

pectinate ligament

ciliary process

lens

adipose pad
optic nerve

Fig. 150 — Seal eyes, x 1. After Putter,
a, an eared seal, Otaria jubata. b, a true seal, Phoca vituli,

In view of the diurnality of the group, the apparent nocturnal adap-
tations of the pupil, retina, and chorioid seem paradoxical at first
thought; but this paradox is the very heart of the method by which the
seal accomplishes amphibious vision. The retinal rods are exceedingly
long and they are commonly said to have no cones amongst them; and
the retina is backed by a bright chorioidal tapetum over much of its area.
These features bespeak a sensitivity which appears totally unnecessary,
at least to the shallow-swimming Otariidas. The reason for it is complex
but fascinating :

In both seals and sea-lions the pupil gives some evidence of being
under voluntary control, but it is ordinarily a very large circle as long as
the eye is under water. The dilatator is so conspicuously developed that

AMPHIBIOUS MAMMALS 447

some of its fibers even lead into the ciliary processes for anchorage.
There is a massive sphincter, equalled among other mammals only by
that of Lutra, and so arranged that the pupil can close to a short and
narrow sUt, about one millimeter by four — and does so, as a rule, the
moment the head comes above water. The slit is vertical excepting in the
bearded seal (Phoca barbata) , where it is set almost horizontally — really,
diagonally with the lower end toward the temple. Possibly in barbata it
is normal to the water surface when the animal rears up, just as the oppo-
sitely-slanted palpebral fissure of turtles becomes parallel to the water at
such times. The walrus forms an exception in that its pupil is always a
broad horizontal oval like that described (by some) for the manatee,
which is comprehensible in view of the similar sedentary feeding habits
of the walrus.

It is reasonable enough for the pupil to close down when the eye is
suddenly exposed to somewhat brighter light upon being lifted into the
air — the same phenomenon is seen in the sea-snakes, for example. But
why close so far, and why to a slit? Why are a nocturnal retina and a
tapetum necessary for vision to continue, out of water, in the seals? They
are diurnal and arhythmic in habit. There is no explanation of the matter
in the literature, but at least there is a clue : Years ago, Lindsay Johnson
puzzled over the astonishing degree of astigmatism which he found in
both seals and sea-lions. Out of water, and under the influence of a
cycloplegic drug — that is, one which dilates the pupil and paralyzes the
accommodation — they showed four diopters of myopia in the vertical
meridian and thirteen diopters in the horizontal, resulting in nine
diopters of astigmatism against the rule (/. e., with a vertical axis) as
though the animals were wearing four-diopter spherical spectacles with a
nine-diopter cylinder superimposed, the axis of the cylinder upright. All
of this refractive error resides in the cornea, hence of course disappears
in water.

In the preceding chapter we learned the virtues of a stenopaic aperture
(pp. 255-6). The ideal one is the pinhole; but no vertebrate pupil which,
when dilated, is a very large circle (as in the seals) can easily close to a
very small pinhole. The nearest approach it can make is a slit. A slit will
focus an object-point as a line which will be parallel to the slit. A cylin-
drical, astigmatic lens will, at its second focal plane (see Fig. 13, p. 28),
image a point as a line perpendicular to the axis of the cylinder. So, if a
slit pupil lies parallel to an astigmatic axis, the combination will image a
point as a point, and will thus eliminate the astigmatism of the whole

448 ADAPTATIONS TO MEDIA AND SUBSTRATES

dioptric system as effectively as a pinhole could do. At the same time, it
will admit more light than will a pinhole of the same width as the slit.

The primitive seal, seeking a means of obtaining sharp images in both
water and air, may have considered the usual method — that of the turtle,
cormorant, and otter — but decided that it involved too much intra-ocular
work to employ both ciliary muscle and iris sphincter to wring the lens.
Much simpler to develop just enough accommodation to give himself
emmetropia under water, and eliminate entirely the need of any great
reserve of accommodation for use in seeing through the air. To make
extensive accommodation in air unnecessary, he developed a high degree
of corneal astigmatism, with its axis and his slit pupil so oriented as to
give an approach to the performance of a pinhole camera. The quasi-
pinhole reduced the retinal illumination so greatly in air that a sensitive
retina, backed even by a tapetum, became necessary. Under water, the
corneal astigmatism conveniently vanishes and the spherical lens, oper-
ated by a quite ordinary ciliary body, goes into action. Its accommo-
dation has now to combat the hypermetropia which replaces the aerial
emmetropia or myopia. The widened pupil lets in enough of the dimmed
subaqueous light, and the seal eye is then as useful in deep water as that
of a shark.

We may be sure that the system works, if not always (Phocd barbata!)
just in this way. Considering their food and feeding habits, seals would
starve without clear underwater vision. On land or ice, a seal is decidedly
alert — not wholly because of his excellent olfaction. He is visually alert,
never sleeping for more than four minutes at a time. True, the elephant
seal appears near-sighted out of water, like a penguin; but even the most
eye-minded vertebrates have a deadline, located afar by fear or nearby
by fearlessness, to which they will allow approach without showing alarm
even though they see clearly far beyond it. The elephant seal's apparent
aerial myopia may really have such a basis. Under water his vision is
surely good, for he feeds on swift cuttlefishes. In great contrast to
Macrorhinus, the average seal will take flight from a man 150 yards
away.

Even a wild seal is reputed to catch in its mouth a stone tossed to it.
The reader may not want to believe this — and can hardly be blamed.
But if he has ever watched a trained sea-lion on a dry stage going through
a repertoire of catching balls, sticks, and finny rewards, he cannot doubt
that the seals in general are as eye-minded, as readily able to see well
through air, as he himself.

TYPES OF SPECTACLES 449

(D) The Spectacle

Injurious Substrates — ^As long as a vertebrate eye is held and pro-
pelled in such a way that only clean air or clean water ever ordinarily
touch it, it may be adequately protected by the glandular and palpebral
devices discussed in Section B, But there is only one ecological type of
vertebrate that normally never encounters a substrate which is potenti-
ally, at least, injurious to the eye. This is the completely pelagic fish —
the free balloon of the vertebrate kingdom. Every other kind of creature
must stay on a substrate, either under air or under water, or at least come
down to that substrate at more or less frequent intervals.

Where the animal's size, structure, or feeding habits place the eye in
intimate relation to that substrate; and where the latter is sandy, muddy,
or beset with protrusions, the Udless eyes of a fish or even the lidded ones
of a land animal may be prone to injury. Where vertebrates have found
themselves in such predicaments, they have usually gotten out of them
by developing protective goggles.

Types of Spectacles — ^Wherever we find an eye which is free to rotate
under a fixed, transparent covering through which it sees unimpeded, we
may call that covering a goggle or spectacle. Among spectacles we can
distinguish three types: primary, secondary, and tertiary. The first of
these is formed by material which, though it ordinarily forms a part of
the eyeball itself, has never become attached and permits the eyeball to
turn freely underneath it. Secondary spectacles are anatomically prac-
tically identical with primary ones; but they represent a secondary split-
ting-off of the material of the spectacle from an eyeball to which it had
long been joined in the ancestors. Tertiary spectacles represent distinctly
extra material overlying a complete eyeball. We may recognize one or
two movable coverings as tertiary spectacles, since they seem to have
been historically antecedent to the latter; but we shall not include the
nictitating membrane even though this is perhaps primarily spectacle-like
in usefulness in one or two cases, as in the horse.

Primary Spectacles and the History of the Cornea and Con-
junctiva— The primary spectacle is seen only in lampreys and strictly
aquatic adult amphibians, and as a temporary affair in amphibian tad-
poles (Table XI, over). It will be recalled that eyelids, where these are
present, are lined with a continuation of their outer skin which is called
the conjunctiva and which, far back under each lid, turns upon itself to

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PRIMARY SPECTACLES

451

form a cul-de-sac and comes forward again to fuse onto the anterior
surface of the eyeball.

The epidermis of this special conjunctival skin continues over the
cornea, slightly changed in the direction of a greater regularity of cell-
arrangement, to form the corneal epithelium. If we seek the dermis be-
longing thereto, we find it not — for it has become the outer layers of the
substantia propria of the cornea (Fig. 151a, b). This augmentation of the
cornea, by the fusion to it of a layer of skin, was not a part of the orig-
inal plan of the vertebrate eye at all. The original cornea was composed
entirely of fibrous connective tissue and was simply the skin-ward por-
tion, kept transparent throughout Ufe, of the dural envelope enclosing
the retinal cup. It quickly received two additions during early vertebrate
evolution — an inner one contributed by the mesothelium of the anterior

Fig. 151 — Comparative morphology of the cornea, the conjunaiva,
and the three categories of speaacles.

a, the primitive situation as exhibited by the lampreys. The primitive cornea pc is a con-
tinuation of the sclera, sc, and moves freely beneath a primary speaacle, which is merely
a transparent window in the head skin sk- b, in other fishes, the skin has fused with the
primitive cornea to form the definitive cornea, dc. Between a distinct margin m and the
eyeball, a deep sulcus s creates a fold of skin which forms a 'conjunctiva fixa' where it
joins the eyeball and a 'conjunaiva libera' where it lies free to permit rotation of the
eyeball. A line of demarcation can still be made out between the primitive cornea and its
new addition, and a secondary splitting of the cornea along this line will create a secondary
spectacle, anatomically similar to the type shown at a. c, the situation in land animals;
lids (/) have formed, so that the conjunaiva is differentiated into a conjunctiva palpebrae
(cp), conjunaiva libera (c/), and conjunaiva fixa (c/). Beneath the lids are deep fornices
or culs-de-sac (cds). The cornea, c, now shows no evidence of the dual origin of its sub-
stantia propria, d, the tertiary spectacle, sp, as seen in snakes and in some lizards and
fishes, has been created by the edge-to-edge fusion of horizontal or vertical lids. Between the
speaacle and the cornea c there is now a blind intraconjunaival space, ics, derived from the
culs-de-sac of the lidded ancestor. This space is lined throughout by epithelium (stippled).

452 ADAPTATIONS TO MEDIA AND SUBSTRATES

chamber and its basement (Descemet's) membrane, together with per-
haps some connective tissue outside of the latter and homologous with
the iris stroma; and an outer addition of skin whose epidermis became
the corneal epithelium and whose dermis merged and fused with the
outer surface of the original dural (sclerotic) tunic, which the retinal
cup had carried outward with it when it grew away from the side of the
brain (see p. 119).

Before this second addition was made, the eyeball had been required to
remain below the level of the skin and to look out through a flat window
therein. This is still the situation in lampreys (Fig. 103, p. 258), which
are too primitive ever to have produced a conjunctiva — a conjoining of
skin and eyeball. The field of vision is restricted just as is that of a man
who looks through a closed window. If he opens the window and puts
his head out, he can see much more.

The higher fishes could not open the window, but they could bulge it
outward — make a bay-window of it, so to say. Friction on the eyeball
being then intolerable, it was expedient to fuse the window onto the eye,
retaining rotability by simultaneously producing, around the window, a
deep circular infolding of flexible, membranous skin so that slack could
be allowed to permit of turning the eyeball.

Thus the conjunctiva came into existence. The addition to the cornea
was coincidental, and not produced for its own sake. The circular fold
of skin overlapping the cornea all the way around proceeded to come in
handy, as when the eye of a ray, for instance, is hauled back into the
orbit by the retractor bulbi muscle, and the skin puckers together over
the eye and protects it. Land animals found that a much neater arrange-
ment was possible, by extending the superior and inferior margins of the
fold to form permanent upper and lower lids. All of them, in their em-
bryonic development, still form their lids from a circular, at first con-
tinuous, fold. These lids being opaque and shutting off vision whenever
they are closed, some animals have added a third, almost or completely
transparent lid, made by folding the conjunctiva in the nasal corner of
the eye and pulling this fold — the nictitating membrane — laterally over
the cornea by special means (Fig. 142, p. 420).

The triple origin of the definitive vertebrate cornea cannot ordinarily
be made out in a histological preparation. The human cornea, under
the slit-lamp microscope, does show a superficial extra-clear layer under
the epithelium which may represent the dermal contribution to the sub-
stantia propria. The connective-tissue fiber-bundles are here somewhat

SECONDARY SPECTACLES 453

differently felted from what they are deeper in the corneal thickness;
but a vertical section through the corneal thickness shows no line of
demarcation in the substantia propria.

In the fishes, however, it is extremely common to find such a line, and
to find that the fresh cornea can readily be peeled apart along the in-
ternal boundary surface which the line represents (Figs. 67 ^ 105a; pp.
159, 261). It is apparently this incompleteness of fusion between the
original cornea and its dermal addendum which has made it easy for
many fishes and some amphibians to produce 'secondary' spectacles,
which actually represent a regression to the anatomical condition in the
lampreys. Even in the highest vertebrates, the corneal epithelium oc-
casionally remembers all too well its origin as head-skin epidermis. Sheep
have been known to exhibit a cornea completely covered with wool.

Secondary Spectacles — These are definitely associated in many cases
with the habit of coming out of water into dry air, or of groping for food
on a sandy or muddy bottom. Secondary spectacles occur in practically
all amphibious fishes, and in a host of bottom species. The secondary
spectacle is never homy like a tertiary one, however, and cannot offer a
cornea so good a protection against desiccation. Moreover, since many
bottom-feeding fishes have small, poorly developed eyes, it is impossible
to say which small-eyed forms have split off a spectacle from the cornea
as a positive adaptation to serve a special purpose, and which possess a
spectacle as an embryonic arrest, as an evidence of a tendency of the eye
to degenerate. For cave salamanders, it is particularly easy to say that
the adult has a spectacle because the degenerate eye has been halted in
an embryonic condition — the primary spectacle never becomes a part of
the eyeball in cave forms as it does, at metamorphosis, in other salaman-
ders. Too little is known of the mode of development of secondary spec-
tacles in fishes — certainly many arise through an embryonic failure of
fusion rather than a secondary splitting of the cornea after fusion. Such
spectacles would be secondary only in the sense of a phylogenetic delami-
nation of the cornea, the fishes having superimposed an inhibition upon
the fusion-tendency which their ancestors permitted to operate. There is
however some suggestion that many piscine conjunctivae are fused and
later separated during development, in the fact that there are usually
some connective-tissue strands crossing from the surface of the residual
cornea to the inside of the spectacle — such very tenuous and elastic
strands (Fig. 152a, st) that the spectacle is able to remain motionlessly

454

ADAPTATIONS TO MEDIA AND SUBSTRATES

fixed in the head skin while the cornea slides under it with the rotational
movements of the eyeball.

A half-way stage in the production of a secondary spectacle seems to
be exhibited by certain of the Cottidae — Ascelichthys rhodorus for ex-
ample. Here, the usual circumocular sulcus (Fig. 151b, s) has been elim-
inated. All that remains to represent the formerly infolded conjunctiva
is a narrow zone of puckered skin surrounding the cornea and merging
with the head skin at the rim of the orbit. The circular, concentric pleats
in this skin afford the leeway required when the eyeball turns in the orbit.
If the surface layers of the cornea continuous with the skin should split
off, the pleated zone could then shrink in area and obliterate its pleats.
Ascelichthys would then have a typical secondary spectacle.

Fig, 152 — Types of spectacles in teleost fishes. After Hein.

a, secondary spectacle of Anguilla angiiilla. ep- epithelium of spectacle (= original corneal
epithelium); sc- separated portion of cornea, forming mass of spertacle; st- strands of
delicate conneaive tissue, which do not interfere with the movement of the eye beneath the
spectacle; pc- primitive cornea, which remains continuous with sclera, b, tertiary spectacle
and eye (collapsed) of Engraulis sp. c- cornea; e- epithelial lining of: ics- intraconjunctival
space; s- sclera; sk.- skin of head; sp- spectacle.

Tertiary Spectacles in Reptiles — The tertiary spectacle is a type
with which most of us are familiar, for we have all noted the glassy stare
of the reputedly lidless serpent. The snake does have lids; but they have
been closed for all time, and converted into the hard, horny, dry trans-
parent, insensitive eye scale of the herpetologists (Fig. 15 Id). There was
long a debate as to whether this spectacle represented the upper and lower
lids, the lower alone, or the nictitating membrane or third eyelid inherited
from the lizards. Recent embryological work on the European grass
snake and on one of the rattlesnakes has shown that after the formation

TERTIARY SPECTACLES IN REPTILES

455

of a circular lid fold — just as in any land vertebrate — this fold gradually
closes in over the eye, the aperture surrounded by it shrinking to the
vanishing point and moving dorsally the while (Figs. 153, 154). Thus it
is manifestly the lower lid which contributes the greater part of the spec-
tacle. In the rattlesnake, the lid opening even becomes a normal hori-
zontal palpebral fissure before it closes, like a healing wound, leaving
no scar or trace in the finished goggle. In one snake, Rbinopbis, a small
slit is still present in the newborn young. Though it is now certain that
the nictitating membrane does not even start to develop at all in the

Fig. 153 — Embryological formation of spectacle in a snake, Natrix tiatrix.
After Schwarz-Karsten.

A circular lid-fold grows, in over the cornea, its aperture at first large and concentric (upper
left) but shrinking and taking up a dorsad position (lower right), eventually closing com-
pletely before birth. The finished tertiary spectacle thus comprises chiefly the lower lid,
the upper lid making only a small contribution and the nictitans none at all.

snake (let alone form the spectacle), it is still a puzzle that the tear-
gland associated with the upper and lower lids, the lacrimal, should be
absent in snakes while the one which lubricates the third eyelid in other
vertebrates — the oily Harderian gland — should be present. The Harder-
ian secretion flows into the space between the deUcate one-layered cor-
neal epithelium and the spectacle, and drains through a duct into the
nose, then into the mouth to mingle with and supplement the saliva.
It is possible that the fluid has a high refractive index and some optical im-
portance, but the optics of the tertiary spectacle remain to be worked out.

456

ADAPTATIONS TO MEDIA AND SUBSTRATES

It is also possible that the snakes, being under the necessity of lubricating
the apposed surfaces of the cornea and the spectacle, elected the Hard-
erian gland simply because of the superiority of oil over water as a
lubricant.

In both snakes and spectacled lizards, an outer layer of the spectacle
is periodically replaced whenever the skin is shed. This renewal of the
surface often comes none too soon — as one appreciates on observing the
sadly scratched and dull appearance of the spectacle of a garter snake

Fig. 154 — The ophidian eye and its accommodation.

a, eye of European grass snake, Natrix natrix, in vertical section, x 22. Redrawn from
Schwarz-Karsten, modified from original preparations.

am- accommodatory muscle, forming sphincter-like mass near root of iris; ap- anterior pad of
lens; t- brain; c- cornea; c^- ciliary body (devoid of muscle); cr- cranium; c^- canal of
Schlemm; hg- Harderian gland; to- infraocular scale; s- sclera (entirely fibrous — no cartilage
or bone) ; sm- sphincter muscle of pupil; so- supraocular scale; sp- spectacle; z- zonule.

b, anterior segment of Coluber <esculapii, in relaxation, x 5. Redrawn from Beer.

c, same as b; in accommodation under electrical stimulation; note forward movement of lens
and decrease of eyeball diameter at limbus (the dome of the cornea has been cut away,
but this does not alter the course of ophidian accommodation).

TERTIARY SPECTACLES IN REPTILES 457

inhabiting such an abrasive place as a stone wall. The formation of a
milky film under the soon-to-be-shed stratum corneum of the skin, all
over the body, can be particularly easily noted in the transparent spec-
tacle, and has given rise to the widespread belief that snakes are blind
when about to moult. The animal stops feeding, seeks water to soak the
loosened comified layer, and is irritable and sluggish; but how much its
vision is actually dimmed is a moot point.

Outside of the snakes, the tertiary spectacle as an adaptation to loco-
motor substrates is found only in two turtles (where it is a temporary
goggle, like a nictitans) and in a few families of lizards. Though no

Fig. 155 — The possible ancestor of the permanent tertiary spertacle: the fenestrated lower
lid of a desert lizard, the scincid Mabuia vittata. x 6. After Schwarz-Karsten.

//- upper edge of lower lid; ul- lower edge of upper lid; w- window in lower lid.

embryological studies have yet been made, it appears to have been
formed here from the lower lid also — at least, what seems to be a half-
way stage is seen in those deserticolous skinks and lacertids which have
clear windows in their lower lids (Fig. 155), as do the turtles mentioned
(Emyda granosa and Chelodina longkollis) . When we examine the liz-
ards for ecological correlations with the spectacle, we find that essentially
two habits seem to have demanded its production: burrowing, and noc-
tumality. The former we can readily understand; for whether the lizard
remains perpetually under firm ground or has only the problem of loco-
motion through shifting sand, poking the head up now and again, the

458 ADAPTATIONS TO MEDIA AND SUBSTRATES

animal would be in misery without a spectacle — at least, so long as the
eyes were retained in useful condition.

In some blind burrowing lizards (e.g., Amphisbaenidae) , the tertiary
spectacle might seem a mere sign of ocular degeneracy — as a secondary
spectacle so often is, in limicolous fishes. But if we imagine the evolution
of a burrowing reptile, we see at once that the spectacle would have to
antedate the blindness, and that it must have been truly protective at
first. Later, of course, the spectacle came to have no meaning — when the
organ it had been protecting degenerated beneath it. A morphological
equivalent of the tertiary spectacle (but one which never was trans-
parent) is seen in some moles, in which the lid opening has constricted
to the vanishing point, leaving the furry skin unbroken over the vestigial
eye. Similarly, in one cave salamander — Typhlotriton spelceus — the lids
develop at metamorphosis, as usual, but then fuse edge-to-edge (except
at their very centers) over the eye. Such opaque spectacles are in quite
another category from those of burrowing reptiles which still had func-
tional eyes long after they had evolved their spectacles.

The spectacles of nocturnal, non-burrowing lizards call for still an-
other explanation. Geckoes* and night lizards (Xantusiidae) may hide
under objects, but they are not true burrowers. Most of them live far
from deserts, and the desert xantusiids live under boulder flakes or in
yucca tops — not in the sand. Moreover, other reptiles such as Spbeno-
don, the beaded lizards, and the crocodiles are just as nocturnal, yet have
normal lids. These latter forms are large-bodied, however; and the an-
swer to the gekkonid or xantusiid spectacle is seen in the fact that these
little chaps place their eyes in constant jeopardy from gravel and stubble,
amidst which they crawl under such poor visual-acuity conditions that
they cannot possibly see them clearly enough to avoid them.

The spectacles of some serpents might seem to explain themselves as
do those of bottom fishes, Emyda and Cbelodina, or the lizards: some
snakes feed in mud, some burrow, some are nocturnal. All of them rep-
tate or crawl with the eyes very close to the potentially injurious sub-
strate. But so do many diurnal lizards, and these have no spectacles.
Most snakes are diurnal and live in above-ground habitats. Many of
them are arboreal, and some are permanently aquatic. Why then do all
snakes have spectacles when only a small minority really need them?
Manifestly, because the original snake or its immediate lacertilian an-
cestor was nocturnal or subterranean. We shall see later (Chapter 16,

*The 'eublepharids' have mobile lids fringed with stiff lash-like scales.

TERTIARY SPECTACLES IN FISHES 459

section D) that the 'first snake' must indeed have lived underground,
and for so long a time that the eyes degenerated very gravely. When the
snakes later became a diversified, largely above-ground and diurnal
group, they all had perforce to keep their spectacles whether they had
any particular need for them or not.

As long as its surface is capable of being renewed, a tertiary spectacle
is clearly more desirable for any land animal than is a pair of movable
lids. We ourselves would be better off with one, and it is perhaps unfor-
tunate that none of our direct ancestors ever had habits which made a
tertiary spectacle mandatory. We are forever getting 'something in the
eye' — and when this happens, we are able to deal with the situation only
because we have intelligent fingers. A wild animal, in the same predica-
ment, may claw its eye until it is injured beyond repair.

But, it would seem that nature can be persuaded to seal the terrestrial
vertebrate's lids, and make them into a spectacle, only where the eyeball
is imperilled far more seriously than it ever is in the vast majority of
lidded vertebrates.

Tertiary Spectacles in Fishes — Spectacles assignable to this category
occur in a few teleost fishes, where they differ from those of snakes and
lizards in almost every particular excepting the most fundamental one
of diagrammatic morphology.

In contradistinction to the secondary spectacle, so widespread among
bottom forms, the tertiary type occurs only in a few pelagic fishes which
are mostly close relatives of fishes in which vertical lids (p. 383) are con-
spicuously developed. Ichthyologists have apparently assumed that all
intact coverings over piscine eyeballs represent closed, fused, vertical lids.
Some taxonomic descriptions of fishes forthrightly call the spectacle,
whether primary, secondary, or tertiary, an 'imperforate adipose lid'.
Clearly, there is need for a more careful identification of types, as other-
wise some gravely erroneous taxonomic conclusions might be drawn.

Externally, in fishes, there is no way to distinguish the three types of
covering. Histologically, the primary and secondary types are discrimin-
able only on the basis of the absence or presence of an intermediate
system of delicate strands connecting the spectacle with the functional
cornea (Fig. 152a). Where these strands are particularly strong, it may
be possible to see them grossly upon cautiously reflecting the circumcised
spectacle from the cornea. Some have claimed to find such connections
between the two structures even in lampreys. However strong or weak
these connective-tissue strands may be, they never prevent the cornea

460 ADAPTATIONS TO MEDIA AND SUBSTRATES

from rotating somewhat under the spectacle, and the presence of eye
movements associated with a motionless spectacle should never be taken
as proof that the spectacle is not of the secondary type.

Histologically, the secondary and tertiary types are more easily told
apart with certainty. It is obvious that if the spectacle of a given fish
represents a pair of vertical lids whose aperture has been entirely abol-
ished, there can be no connective-tissue strands crossing the space be-
tween cornea and spectacle. More important still, there is bound to be
a thin epithelium lining this space, covering the cornea (where it repre-
sents the corneal epithelium — stratified, of course, in other fishes) and
continuing over the inner surface of the spectacle, where it represents the
epidermis of the palpebral conjunctiva (see Fig. 15 Id, p. 451). Such a
situation has hitherto been reported for only one fish. Some years ago
a Dutch investigator, Hein, described and figured an epithelium-lined
subspectacular space in a clupeoid, Engraulis sp., and suggested that the
same situation might obtain in certain other fishes, specimens of which
he was unable to obtain for sectioning (Fig. 152b, p. 454).

The writer has been unable to see an epithelium on the cornea, or
lining the spectacle, in sections of small museum specimens of Engraulis
mordax kindly furnished by Dr. Hubbs; but he has found it in the 'pre-
herring' Chanos chanos, and is willing to assume that the spectacles of
the anchovies and their near relatives {Ancboviella and Engraulis; Etru-
meus) are likewise of the tertiary type. The smallest specimens of such
fishes fail to show any aperture in the spectacle, which thus either closes
before hatching or is intact from its first appearance in the embryo.

In an acanthopterygian fish (Polydactylus octonemus) , also, the writer
has found the crucial epithelium. Here, it apparently consists of two
layers of extremely flattened cells — in Chanos, there is but one layer, as
in spectacled reptiles. Presumably the spectacles of any fish of the group
to which Polydactylus belongs (the percoid family Polynemidae) would
reveal the same epithelial lining and completely empty subspectacular
space. There is one clupeoid, however, whose condition cannot be so
confidently predicted. This is the aberrant Gonorhynchus, which, though
related to families which have vertical lids or tertiary spectacles, is
catfish-like in habitus and habits. The spectacles of Gonorhynchus may
prove to be of the secondary type, rather than the tertiary.

These teleostean tertiary spectacles have certainly originated from
paired, independent, 'adipose' lids which have fused edge-to-edge. Their
tissue is of the same sort, and they are likewise devoid of an epidermal

TERTIARY SPECTACLES IN FISHES 461

epithelium on the surface presented to the water. Those clupeoids which
have them are next-of-kin to the herrings and their relatives, in which the
vertical lids are well-nigh universal (see p. 383, Fig. 132). Functionally,
tertiary spectacles are streamlining devices par excellence, no doubt a bit
superior to the independent fore-and-aft lids from which they arose.
Like the vertical lids themselves, tertiary spectacles have been separately
evolved by both malacopterygian (clupeoid) and acanthopterygian fishes
— always in adaptation to the habit of swift swimming, in contrast to
the secondary spectacles which so much resemble them, but are charac-
teristic of sluggish benthonic species.

Chapter 12

ADAPTATIONS TO PHOTIC QUALITY

(A) Color Vision in Animals

The Limits of the Spectrum — The first and foremost adjustment of
vertebrates to the quality (that is, frequency) of light, as opposed to
its quantity or intensity, was the positioning of the limits of the visible
spectrum. When a student first learns that the visible spectrum occupies
barely a single octave on a great keyboard of radiant-energy frequencies,
he may well wonder why the eye evolved with such narrow limitations
of its capacity. Since all sorts of organic substances exist which are
absorbent of {i.e., opaque to) frequencies far beyond the visible band
in both directions, could not a much more broadly sensitive retina have
been as easily devised, so that we could see much more in the world with-
out benefit of fluoroscopic screens and infra-red-sensitive camera films?
Such a retina might have evolved, but not where the vertebrate eye
took its origin — in water. Of what point to an aquatic eye, to evolve
sensitivity to lights which can never strike it? By Visible spectrum' we
usually mean the assortment of contiguous wavelengths which stimulates
the cones. This spectrum has complexities — of limits, peaks of maximal
stimulating value, etc. — due to the behavior of the color-vision mechan-
ism, which is far from primitive and, in land animals like ourselves, has
been partly released from slavery to the properties of water. What the
really primitive, pre-color-vision cone spectrum may have been like, we
cannot know; but the next-most-ancient absorption spectrum is that of
fish rhodopsin, which in its shortening at the red end and in the position
of its maximum is clearly adjusted to the kind of light in which it has
to operate. It is thus no mere coincidence that the risible spectrum is
roughly the transmission spectrum of water. The rod spectrum is closely
fitted to water, the cone spectrum a little better fitted to air.

Value and Origin of Color Vision — But the fitting of the sensitivity
of the eye to the kind of light available is not the most conspicuous
adjustment to photic quality. It is overshadowed by 'color vision', by
which we mean the capacity to respond differently to lights which differ
only in frequency. Where vertebrate color vision is a conscious process,

462

VALUE AND ORIGIN OF COLOR VISION 463

as it is in most cases and possibly in all, it involves differential sensations
with respect to frequencies or imitative combinations of frequencies —
mixtures which arouse the same sensations as single frequencies or other
mixtures (see pp. 81-102).

In science, questions which begin with the word 'what' are supposed
to come first, to be followed by 'how' questions — 'why' queries being
left largely to the philosophers. We know a great deal about the 'what'
of color vision. But we know exasperatingly little about its 'how'. It is
about as profitable, in the present state of knowledge, to spend thought
upon its 'why':

For human beings, color vision has largely aesthetic values. If it is
present in lower animals, which certainly cannot appreciate sunsets and
old masters, what does it do for those animals? What was the incentive
for its evolution? We cannot answer this question simply by comparing
our chromatic, daylight vision with our achromatic experiences by
moonlight, for too much else besides color is missing in the latter. But
if we compare a black-and-white motion picture with one in color, we
note at once a great difference in the visibility of things in the two^ The
black-and-white cameraman must be ever alert to maintain sufficient
contrast. The heroine may report for work wearing a red blouse and a
blue skirt. The cameraman may have to order one of them changed, if
she is not to appear, on the screen, as if wearing a uniform! There may
actually be more contrast in her costume, as far as the black-and-white
film is concerned, if she wears two shades of the same color.

Color vision, then, promotes the perception of contrasts and hence,
visibility. It cannot make vision capable of such complete analysis as
audition (where every tone is a 'primary') can accomplish. But it does
add a hundred and sixty qualities to human vision. To the first animals
which developed a system of color vision, it meant the life-saving differ-
ence between being sometimes able to discriminate enemies and prey
against their backgrounds, and being usually able to do so. 'Conceal-
ment coloration' is a counter-adaptation of some animals against the dis-
guise-piercing searchlights of other animals' color vision; but if its evolu-
tion and perfection had ever caught up with color vision itself, zoologists
would probably not be here to worry over either phenomenon.

The Duplicity Theory (Chapter 3, section C; Chapter 7, section D)
expresses the association of color discrimination with cone visual cells.
We shall see shortly that there is reason to suspect that this part of the
Theory does not hold at all universally; but at least no pure-rod animal

464 ADAPTATIONS TO PHOTIC QUALITY

has yet been clearly demonstrated to have color vison. The tieup of cones
and color vision is entirely to be expected and is not accidental. Rod
vision, in the vast majority of nocturnal and twenty-four-hour animals, is
even much more diffuse and unclear than in ourselves. Where visual
acuity is so low as to be little more than movement- and silhouette-per-
ception, contours and contrasts are so ill-defined to begin with that per-
ceived color-differences could add nothing to visibility. There were
almost certainly cones before there were rods, but there was probably no
color vision in the vertebrate world until retinal and general ocular struc-
ture had progressed to the point where an optical basis for decent visual
acuity had been laid. So, when color vision did arrive, it was only logical
that it be installed in the cone mechanism. Even if the acuity of rod vision
were always equal to that of cone vision (which seems to be true only of
the frog), the operation of Weber's law (p. 534) would still lead to fatal
reductions of contrast in the intensities of illumination suited to rod
activity. Color vision could be of value only in the photopic visual mech-
anism of animals with diurnal activities.

The retinal mechanism of human color vision may be much simpler
than we are fond of imagining; but on the assumption that the human
retinal process is complex — so much so that it must have evolved step by
step over a painfully long period of vertebrate history — ^biologists have
long been interested in the question of where, and in what degree of com-
pleteness, color perceptions first appeared, like Christmas decorations,
upon the phylogenetic tree. Psychologists have hoped, firstly, that by
working out the color-vision systems of a series of vertebrate types, they
might be able to identify simpler systems than the three-primary or tri-
chromatic human one, which would then represent stages through which
the human system evolved. The various dichromatic or other reduction
systems of occasional humans might then be interpretable as atavisms.
And, secondly — ^holding the quite unwarranted conviction that the
chromatic photochemical system must have differentiated from rhodopsin
— they have hoped to find, in the retinae of lower animals, chemical way-
stations which would justify the assumptions of one or another of the
metabolic or genetic theories of human color vision, such as the elaborate
ones of Hering and Ladd-Franklin.

Before the discovery of visual-cell transmutation in 1934, the first of
these hopes was quite reasonable. It may still be, and the color-vision
tenet of the Duplicity Theory — that only cones can mediate color vision
and that no rods do so — may hold quite strialy for all vertebrates, for

VALUE AND ORIGIN OF COLOR VISION 465

all we can say at present. But with transmutation (pp. 163-8) in mind,
we know that we must be less ready than ever before to assume this, and
we must realize that even if a series of color-vision systems is ever found
in vertebrates, only a far more accurate knowledge of the course of phy-
logeny than we now have can ever make it possible to say which simpler
systems are stages in the evolution of human color-vision, and which of
them are independent inventions.

For, just as it is certain that rhodopsin has been invented many times,
it is almost certain that color vision has been repeatedly evolved in differ-
ent vertebrate groups. When the geckoes' rods were secondarily made
from ancestral lizard cones, was color vision lost? If so, then has it
returned in the tertiarily diurnal gecko Phelsuma? Do snakes have
color vision — and if so, could it conceivably have been inherited directly
from the lizards through the snakes' underground, degenerate-eyed begin-
nings? Did those first placental mammals keep any of the cones (and
color vision) of their ancestors? Or is it because the cones (and color
vision) of the placental mammals and primitive snakes were reinvented
by those groups, that there are no oil-droplets or double cones among
them as there are in their respective marsupial and lacertilian forebears?
We cannot answer positively any of these questions or others like them;
but every one of them is absorbing to anyone who is both interested in
color vision and convinced of the past occurrence of cone-to-rod and rod-
to-cone conversions.

Withal, the very existence of any capacity for hue-discrimination has
been proven for so very few groups — none of them anywhere near the
direct road of primate evolution — that much pioneering work remains to
be done before anyone need concern himself with 'systems' and their phy-
logenetic significance or lack of it. It would be very fine if a moratorium
on new genetic theories of color vision could be enforced, until a great
many more cold facts have been garnered.

Evidence for Color Vision — The techniques, some of them very in-
genious and some of them very stupid, which have been used to ascertain
whether particular animals discriminate hues, defy classification. All of
them however involve an all-important potential pitfall which at first
went unrecognized, was later disposed of most inadequately by one
means or another, and nowadays constitutes the careful investigator's
most time-consuming concern. This pitfall is the danger of concluding
that the animal has discriminated between two color-stimuli on the quali-
tative basis of hue, when he has actually discriminated them on the quan-

466 ADAPTATIONS TO PHOTIC QUALITY

titative basis of brightness. Nor may it be forgotten that two stimuli,
which diflFer for us in hue and in brightness, may be alike in both hue and
brightness for an animal, and still be distinguishable by him upon yet an-
other basis — saturation. It is on this basis, be it remembered, that the
dichromatic human distinguishes two 'yellows' which to the normal
appear respectively red and green.

There is a certain amount of purely observational evidence for color
vision in some groups of vertebrates which, though it is no proof, is
strongly suggestive and did seem evidence enough to the elder school of
naturalists. Animals, particularly diurnal ones, are often brightly colored;
and there are often sexual differences which are either permanent or
nuptial — associated with the breeding season — as in some fishes, sala-
manders, lizards, and birds. Where the coloration is sexual, it is easy to
assume that it means color vision on the part of the opposite sex at least.
Indeed, this assumption was the very basis of Darwin's theory of sexual
selection. Where gaudy colors are not obviously involved in sexual recog-
nition one may assume that they indicate color vision on the part of the
animal's natural enemies — particularly where we can be at all sure of
concealing' or 'advertising' colors. 'Protective coloration' fools humans,
which it might not do if they were color-blind. It fools the animal's
enemies as well; and so, runs the argument, the latter must have color
vision, and moreover a system much like that of man. Color-changes to
fit backgrounds, while not nearly so common or precise as once thought,
could only mean the possession of color vision on the part of the changer.
Albino and isabelline birds are noticed, ostracized, and killed by their
normal relatives. Though this may imply only intensity-discrimination,
the hoarding habits of magpies, bower-birds, and others indicate a fas-
cination and ajsthetic interest in color as well as brightness. Bulls were
'well known' (before the days of experimental psychology) to be angered
by red objects. The mink is claimed by trappers to be very curious about
anything red, and it has seemed only natural that animals should be able
to distinguish at least this color, since spilled blood can be so important
to them. Finally, the coats of nocturnal birds and mamjnals tend to be
drab and dark. The tacit implication is that such colorations are prim-
itive, and that diurnal species have become dressed more gaudily because
somewhere there are eyes to be confused by, or to appreciate, the colors
which disappear — for all eyes alike — by the light of the moon.

Observational evidence has been sufficient to fuel the fires of many an
argument between anglers, convinced or unconvinced that the color of a

OBSERVATIONAL EVIDENCE FOR COLOR VISION 467

fly means something to a trout; but experimental evidence is more satis-
fying to the souls of scientists and — when it is sympathetically inter-
preted to them — of sportsmen as well. These worthies have suffered
abundantly with the psychologist's disinclination to try to study trout in
small experimental aquaria, and with his warnings to the angler against
assuming that if a mud-minnow has demonstrable color vision, a trout
must have it also.

In our consideration of experimental procedures and findings, it may
be said at the outset that much of the scientific literature itself is largely
or wholly worthless. Almost always this is owing to incaution regarding
the big danger mentioned above. In the work of one prolific investigator
— Carl von Hess — it is also the result of certain assumptions which no
one before or since has deemed it at all wise to make. Even where the
researcher has made only correct assumptions and has been fully awake
to all possible errors of interpretation, he has not gotten far — no one
could — if his method has made use only of unlearned and untrained
responses by the animal. These can be valuable, but only methods in-
volving the training of the animal can be very fruitful, or make possible
anything like a complete analysis of a color-vision system.

If the animal is to be made 'positive' to one of two or more stimuli—
in other words, trained to evidence a discrimination if he can make one
— he must be capable of trial-and-error learning. The angler may be im-
patient with the scientist for spending his time with the wrong species;
but the scientist is as often annoyed by the rigors of his code, which for-
bids him to use any methods but those he considers the best, for this
often prevents him from working upon the very species about which he is
most curious. For if an animal is very stupid, like an opossum or a guinea-
pig, he might have flamboyant colors in his brain, yet we might not be
sure that he had any. If, like a snake, he eats infrequently and responds
to mild punishment for his errors by getting angry, sulky, or flighty, he
may be both highly intelligent and richly color-perceptive; but we may
not be able to help him to prove it by giving him a proper incentive to
work to make discriminations. The animal must get the idea of what is
expected of him, must be willing to work for frequent small rewards, and
must be able to do the task involved in demonstrating a choice between
stimuli to the experimenter.

A Sample Ideal Procedure for Investigation — The reader will un-
derstand better the difficulties involved in really good color-vision
research, and will be able to see for himself the loopholes in some of the

468 ADAPTATIONS TO PHOTIC QUALITY

reports digested below, if an ideal investigation is outlined in some detail :
You wish to discover whether woodchucks, say, have color vision.
Secure your animals, young enough to tame readily, and get them thor-
oughly friendly and used to handling while building your apparatus.
This must be installed in a quiet room, in uniform surroundings so that
no noise, odors, or asymmetrical lighting can serve as cues or be disturb-
ing to the animal. The apparatus will be essentially a long, horizontal
Y-shaped box, big enough so that the animal can be introduced at the
bottom of the Y behind an opaque door, which you can release at your
pleasure to let him amble comfortably down the long leg of the box to
the junction, there turning either to right or left into one of the wings of
the Y. You must be able to tell, visually or otherwise, where he is at all
times; but he must not be able to see you while he is in the apparatus,
else you may inadvertently give him a cue by your position or expression.
As he approaches the junction of the Y he sees lights there, one of which
eventually comes to mean to him that he is to turn toward the side on
which that light is presented — if he can learn that much, as a woodchuck
certainly can. If he makes the proper turn — say, into the right wing —
you release a barrier in that wing which allows him to get at a standard-
sized small piece of some woodchuck candy or other, perhaps carrot.
An identical reward is in the left wing of the box behind a similar
barrier so that olfactory cues are balanced for the animal, but if he goes
to the left you keep up the barrier and shortly return him to the starting
point for his next trial.

You must not ask the animal to make an absolute reaction, only a
relative one. Memory for absolute values is very faulty even for man. At
the jimction of the box there must be two stimuli side by side, both of
which he can see clearly at all times — even after he has made his choice
between them. One of them leads him to food, and is called the positive
stimulus. If he turns toward the side where the other stimulus is, he gets
no food by thus responding to the negative stimulus. The positive stim-
ulus must not be varied in hue or intensity, for if he associates it with
food he will probably become greatly upset and bewildered if it is altered
in hue or brightness. It must, however, be changed in one way, i. e. as to
the side on which it is presented in successive trials. Otherwise the animal
will probably fall into a 'position habit', going always to the right or
always to the left, having really formed the association 'right = food' or
'left = food' instead of the one — 'blue = food', say — you want him to
establish. So, the blue stimulus must be on the right and on the left equal

COLOR-VISION RESEARCH PROCEDURE 469

numbers of times in the long run, but the alternation must not be at all
regular or the animal will probably catch on to that. Some investigators,
using choice-boxes for any sort of comparative psychological work, flip a
coin before each trial to decide which side the positive stimulus is to have.
In the course of a long experiment — and they are always long — there
will be equal numbers of heads and tails.

When the animal has done his daily stint in trials — maybe ten, maybe
a hundred, depending upon his capacity for work and the speed with
which he gets filled up on the amounts of food which are big enough to
interest him as rewards, you let him finish his dinner in his cage in the
next room, and start with the next animal. The animals will get no more
food until the next day's experimental period, ensuring that they will
then be hungry and willing to work. Perhaps the food drive will not
prove sufficient, and you may have to wire the floor of the choice-box so
that you can give the woodchuck a light shock if he turns to the wrong
side. The stimulus with which you shock him will now be the positive
stimulus, and must not be varied; for he will now be making the associ-
ation 'not blue = pain'. If you assume that he associated 'blue = safety',
and change the other stimulus, he may seem to be unable to discriminate
between the two, simply because he no longer knows what to avoid.
Obviously, you must not both reward him for going to one stimulus and
punish him for going to the other, or you cannot alter either and there-
fore cannot find out whether they can be made to look alike to him with-
out looking alike to you.

The stimuli themselves may be squares of colored paper or they may
be patches of light cast on ground-glass screens from behind. If they are
of paper, you can have the advantage of working with fully light-adapted
animals, but it will be harder to make certain that the discrimination is
not on a basis of brightness alone. If they are lights, the room will need
to be darkened. They may be colored by being passed through gelatine,
glass, or liquid filters; or they may be more nearly monchromatic lights
selected by slits from a broad, bright spectrum. In any case no wave-
lengths present in one should also be present in the other. It must be
convenient to alter their intensity over a great range without changing
their hue, though of course only one will be so altered in any given
course of training. This will require changing the distance of the lights
from the screens, or interposing various thicknesses of ground glass or
smoked wedges which do not change the size or shape of the stimulus-
patches.

470 ADAPTATIONS TO PHOTIC QUALITY

Suppose the woodchuck has learned perfectly to go always to the blue
member of a blue-red pair of stimuli. You may now begin changing the
red stimulus in brightness, to look for a point at which the two stimuli
are equally bright to the animal. There is sure to be such a value of in-
tensity of the red light, but if you are fortunate you will not identify it.
If the animal has been discriminating the colors as such, he will continue
to go to the blue no matter how the red may be altered bit by bit, trial by
trial or day by day, up or down, in intensity. If on the contrary he has
been going to the blue only because it was brighter, say, than the red for
his eye (it matters not that the two may originally have seemed equally
bright to your own eyes) , then at some intensity value of the red stimulus
he will break down and make chance scores — that is, go as often to one
stimulus as to the other. On the face of things this will indicate that he
is totally color-blind; but he may only have been paying more attention
to the greater brightness of the blue than to its coloredness. In this case
he will soon make the 'blue = food' association once more, even with the
red stimulus held constant at the confusing value. But if he continues
indefihitely to make chance scores, and goes to the red stimulus when
this is brighter for him than the blue (the 'step-wise phenomenon' —
always going to the brighter, or less bright, of any two stimuli) , then he
surely has no color-discriminatory capacity whatever.

If the two stimuli first used were not from near the opposite ends of
the spectrum, however, the animal might break down at particular inten-
sity-values, and still have color vision, of a diflFerent character from the
normal human. Yellow and orange, or blue and violet, would probably
look alike in hue to an animal with a dichromatic system anything like
that of a 'color-blind' human (see pp. 97-9), whereas either member of
one pair would always be discriminable from either member of the other
pair, since the two pairs are on opposite sides of any possible dichromate
neutral point. Where there is any suspicion that the species in hand is
dichromatic, a search must be made for a neutral point or band — a
spectral region which the animal cannot distinguish from a white light.
But it so happens that no vertebrate species (unless it be the cebus mon-
key— see p. 516) has yet been found to have a dichromatic system,
though unfortunately few investigators have so devised their experiments
as to disclose dichromasy even if it were possessed by their particular
animals.

If colored papers or objects are used, it is most convenient to eliminate
the possibility of a brightness-basis for the discriminations by training the

COLOR-VISION RESEARCH PROCEDURE 471

animal to a color versus a medium gray, substituting other grays from a
finely-graded series after the animal has become thoroughly trained to
the color. If no gray elicits confusion between it and the positive stim-
ulus, then the latter is being seen qualitatively. Several publishers here
and abroad offer long series of colored papers, and gray ones ranging
from pure white to dead black. In some of these gray series, no two
adjacent samples can be told apart by the human, and it is not likely that
many animals (except birds) have any finer capacity for brightness dis-
criminations. Some of your critics, even so, are sure to say that if you
had used more shades of gray, one of them would have confused the
woodchuck which, you insist, can see blue. To silence all critics, one
simply must use colored lights, whose intensities can be very gradually
regulated. It will help though, if you establish that a woodchuck trained
positive to a medium gray cannot identify it alongside of neighboring
shades of gray.

Having established that your animals distinguish the hues of red and
blue, you have made but a bare beginning. You now re-train them to
other pairs of colors and try to find out how many hues they can dis-
criminate as compared with man's 160 or so. By training to darkness
versus a red wavelength, and increasing that wavelength slowly, the limit
of the animal's spectrum can be found at that wavelength which, how-
ever intense physically, is invisible — at the border of woodchuck infra-
red. So, also, the violet spectral limit can be located. In the woodchuck,
it will not be as low a wavelength as that of man, because of the strongly
yellow coloration of the lens of the animal. Systematic pursuit between
the animal's spectral limits, using pairs of wavelengths which are fairly
close together in the spectrum, with the negative hue (after training)
being gradually approximated to the positive one, will enable you to plot
a graph of the rate-of-change-of-hue against wavelength. Comparison of
this with the human curve will be interesting, and may be extremely
valuable to color-vision theories and theorists. Similar examinations of a
series of red-blue mixtures will disclose whether the color circle is closed
by purples for the woodchuck, as it is for man. Perhaps you will find it
possible to detect chromatic after-imagery in the woodchuck — by training
him positive to blue-green, for instance, then seeing whether he gives the
positive reaction to a neutral gray after being fatigued with red. And
of course you will wish to determine his brightness-threshold for various
colors, and to ascertain how color equations hold for him — what mixture
of red and green looks the same to him as a given orange, what mixtures

472 ADAPTATIONS TO PHOTIC QUALITY

are complementary for him, and so on. The animal's threshold of bright-
ness-difference will be nice to know — indeed, this value, determined with
white lights, might be worth doing first of all, for it will give you an
idea as to how much you dare change, at one step, the intensity of a
negative stimulus with which you are trying to confuse the animal in
your search for hue-discriminatory capacity.

Now, no one has done all of these things with any vertebrate species
other than Homo sapiens himself. Even if all of the really careful work
that has been done, on all vertebrates, had been done on some one
species, we would not know quite all of these things about that one ani-
mal. Far from being able to compare color-vision systems, all we now
know positively — from well-conceived experimentation — is that a few
animals do see colors and that a few others do not, and that apparently
the color-seeing forms all have a mechanism much like our own. Obvi-
ously very, very much remains to be done!

In the following review of the experimental literature, the fishes are
dealt with fairly completely — not because their color vision is any more
interesting than that of other groups, but because it is better known and
more different investigators have applied more different methods, with
more different advantages and faults of technique and interpretation, to
its study. The procedures and results with higher vertebrates are describ-
ed more sketchily, since after having a given procedure once character-
ized for him, the reader can be spared any detailed reiterations of favor-
able and unfavorable criticisms.

Fishes — The reader's suspense, if any, may as well be relieved at once
by the flat, if somewhat back-handed, statement that no fish is known
not to have color vision. But the angler can take little comfort from the
fact. As will appear shortly, he cannot predict whether a red fly will
attract or violently repel the fish he is after. In fact, there is every reason
to think that a dry fly, or a floating plug of any color, is seen by the fish
merely as a dark silhouette whose form is much more important than its
hue. Much though we may know of the color vision of laboratory fishes,
and infer as to the color vision of game species, when it comes to wet
flies and plugs the old rule still holds : what they'll take, they take, and
what they won't, they don't.

The first scientific work on fish color vision was reported by Graber in
1884 and 1885. He made use only of untrained responses made by the
fish toward different stimuli presented in pairs — the so-called color-pre-
ference technique. Working with the freshwater Bar ba tula barbatula and

COLOR VISION IN FISHES 473

Alburnus alburnus, later with the marine Spinacbia spinachia and
Syngnathus acus, Graber found a preference for darkness as opposed to
white light, and a decided preference for red light over blue, produced
by glass filters. Equating the colored lights in brightness for his own eyes
(and of course assuming that they were then of equal brightness to the
fishes) , he determined that the animals preferred red to green, and went
to green or blue when either was paired with a blue + ultra-violet (by
which is meant, here and elsewhere in this discussion, human ultra-violet
— that is, wavelengths beyond the short-wave end of the human visible
spectrum. What is truly 'ultra-violet' for an animal may commence at a
longer or shorter wavelength than the one which is just visible to man) .
By making a red light twenty times as intense as a blue one, Graber
could force his fishes to show a preference for the blue.

The earliest use of the method of training seems to have been that of
Zolotnitzky who, in 1901, fed fishes for a time on red midge larvae and
then attempted to deceive them with bits of colored yam glued to a card
which was held against the glass side of the aquarium. The fishes tried
to get at the red pieces, ignored those of other colors. A first attempt to
eliminate the possibility of discrimination on a basis of brightness-differ-
ence was made five years later by Washburn and Bentley, who induced a
*red=food' association in Semotilus atromaculatus by feeding from a
red-marked forceps presented simultaneously with an empty green one.
The dace continued to go to the red forceps even when it contained no
food, and even when the shade of red was changed considerably in either
direction of brightness.

In 1908, Reighard concluded that Lutianus griseus discriminates hues
as such, for he failed to find what has since come to be called the step-
wise phenomenon. Offering both red and blue baits to wild gray snap-
pers in the open sea, he found that they avoided the red ones. They also
preferred white to blue. Back in the laboratory, Reighard found that the
brightnesses of the stimuli he had used were in the order white->red->
blue. Since the fishes preferred the brighter member of one combination
(white-blue) and the duller member of another (blue-red) , he concluded
that they were guided by color rather than by brightness. He was further
convinced of this when he found that fishes negative to red baits refused
all shades of red, at the same time accepting other colors which must have
been matched in brightness for them by one shade or another of red.

From 1909 to 1915, a flood of papers appeared in which the capacity
of fishes for hue-discrimination was debated pro and con, with Hess tak-

474 ADAPTATIONS TO PHOTIC QUALITY

ing the negative side and with first Bauer, later Karl von Frisch, cham-
pioning the positive. The influence of Carl von Hess can hardly be ex-
aggerated, for he devised some ingenious procedures, and helped his
critics to improve their own work by his continual insistence that the
brightness factor was not properly controlled in previous and contemp-
orary work. He himself tended to avoid the use of techniques in which
any control of brightness was theoretically necessary. Some of his
assumptions and interpretations were so repugnant to others, however,
that his work served to stimulate an outpouring of research which might
not otherwise have been done even yet. Being a very great physiologist,
Hess made very great mistakes when he made any at all; and other
investigators were quick to point them out.

Hess used two methods particularly : that of preference, and the study
of the pupil-contracting effects of the colors of lights. His argument was
as follows : The totally color-blind human eye and the dark-adapted nor-
mal eye (which is color-blind) see the green region of the spectrum as
brightest, whereas to the normal light-adapted eye the yellow region of
the solar spectrum is most luminous. This shift in the position of the
peak of maximal brightness is of course the Purkinje shift (Fig. 30, p.
87), and is accompanied by a relative decrease in the brightness of red
and a relative increase in the brightness of blue stimuli on passing from
full light-adaptation toward dark-adaptation, upon reducing the intensity
of illumination. If for fishes (or other vertebrates — or invertebrates!) the
brightest spectral region is the green when they are light-a-dapttd, and if
they show no Purkinje phenomenon, then they are color-blind. If their
pupils close further in response to green light than to other colored lights
of equal physical energy-content, then the green is brightest for them,
and they are therefore totally color-blind. Hess applied this argument
not only to fishes but to a host of other animals as well.

The fallacies inherent in this argument are glaring ones, and the most
important of them have been repeatedly explained by others. There is
no justification whatever for assuming that the curves of spectral lum-
inosity, with or without color-vision, must be the same for any animal as
for the human. The writer would go even further, and insist that an
animal could have color vision and yet have no Purkinje phenomenon —
the latter exists at all, in man or animals, as a sheer fortuity : the peaks
of absorption of the rod and cone photosensitive substances are not iden-
tical in location in the spectrum. If they were identical (and they might
just as well be), there would be no Purkinje shift. The scotopic absorp-

COLOR VISION IN FISHES 475

tion maximum of a fish may be at a wavelength as high as 545 m(l, as
contrasted with the human value of about 510m[X. Should the photopic
maximum of the same fish happen to fall at the human value of A,557m^
(and it probably would) the Purkinje shift would be only 12m|i, instead
of 47m[l; and a downward shift of the photopic maximum could even
bring the two peaks into coincidence. Too, the normal human retina is
totally color-blind in the extreme periphery, yet even here the brightness
values of chromatic stimuli are those characteristic of photopic, not of
scotopic, vision. Thus a Purkinje phenomenon occurs here in the absence
of color-vision. Human dichromates experience an inversion of the
relative brightnesses of red and green, upon a change of adaptation —
yet red and green, for them, are the same hue. They thus have an
'isochromatic' Purkinje phenomenon as compared with the 'heterochro-
matic' one of the normal trichromatic individual.

The argument from pupilloscopic findings is even shakier; for while
in man the pupil is controlled reflexly from the retina and appears to
respond maximally to a given color because that color is consciously seen
as brightest, in the fish any iris muscles are entirely autonomous and there
is no reason to suppose that the wavelength which most stimulates them
will also maximally stimulate one or both sets of visual cells in the retina.
The teleost pupil moves but little at best, and in his examinations Hess
made no attempt to eliminate the passive effects of lens movements upon
its size.

Hess worked largely with very young fishes, apparently in order to be
able to have large numbers (up to 60) in the same small tank, so that
their distribution in the spectrum thrown in the water would be devoid
of crowding-effects, and would also be statistically significant. For this he
has been taken severely to task, as also for making too few control tests
with thoroughly light-adapted specimens, for disturbing these before test-
ing by carrying them for some distance to a darkroom, and for ignoring
certain performances when they failed to confirm his ideas.

With species after species, Hess found that the fry would usually
gather in the green or yellow-green portion of the proffered spectrum
(A,525-535m[x). He concluded that this region looked brightest to them,
since he claimed that they were always step-wise in their preferences for
white lights of different intensities. When pairs of spectral lights were
offered, the choices of the animals determined a curve of relative bright-
ness which simulated that of the scotopic human. Hess claimed to have
eliminated the possibility that this was caused by a Purkinje effect, by

476 ADAPTATIONS TO PHOTIC QUALITY

repeating the findings on light-adapted specimens. He also contended
that the red end of the spectrum is shortened for all fishes (as for the
scotopic normal, totally color-blind, or protanopic human eye) . By driving
the fishes toward the red end of a spectrum with an advancing shadow, he
found that they would still congregate in the light when wavelengths as
short as 620-640m[l were still shining on the aquarium; but when the
shadow reached to 7,650m[A they suddenly dispersed as if they were in
complete darkness. When two lights were shone on the tank from opposite
ends, their relative intensities could be adjusted so that the fishes swam
indifferently through both colors of illumination. With this procedure
Hess found that the green was brightest, that blue, yellow, and orange
were less bright, and that red was darkest for the fish. The intensity of
any color needed to 'balance' pure yellow was only half that required to
balance green. Unlike Graber, he could make his fishes go to red, by
making it far brighter than an alternative blue light.

Bauer worked with Charax puntazzo and Atherina hepsetus, to some
extent also with a species of mullet, and a bit with Box salpa. He used
filters of glass, gelatine, and paper and made a few experiments with
spectral lights. He found that his fishes (except Mugil) were instinc-
tively strongly negative to red (?i680-710m[A) and called this peculiar
phenomenon 'Rotscheu' or red-fear, red-shyness. Reighard had observed
it in Lutianus as noted above, without realizing of course how very many
species would show it. Fishes generally seem either to shun red, or to pre-
fer it decidedly. This paradox does not appear to have interested the in-
vestigators in this field; but, granting that the red is seen as such, red-
shyness and red-love both seem to indicate a high attention-value for red.
Though red is very common in the body colorations of fishes, it is prob-
ably rarely sufficiently illuminated to be seen as anything but black, for
the red rays are the first visible ones to be eliminated as light passes down
through water. Perhaps it is because red, distinctly visible as red, is so
unfamiliar to fishes that it gives them such a start in one way or the other.
Both the shunning and the pursuit of red may mean the same thing —
that the fish sees the red vividly, that it is strange, and that it fascinates
him. Young fish, to which everything is new and strange, seldom ex-
hibit red-shyness; and even old fish may get over it in a short time.

Bauer also established that his fishes were quite indifferent to wide
variations in the intensity of white light. He could not get them to settle
down in either of any two intensities. Yet when offered red and blue they
would go to the blue, and no juggling of the intensities of the two colors

COLOR VISION IN FISHES 477

would bring about an equal distribution of the animals. These findings
were directly contradictory to those of Hess, irrespective of any differ-
ence of interpretation; for Hess had claimed that an intense red and a
blue were responded to alike and perceived alike, and that Atherina
hepsetus responded differently to white lights differing as little as by a
1 : 1.23 ratio in brightness. Later work by others has substantiated Bauer's
contention that the intensity-discrimination of fishes is extremely poor.
Of course, it is probably mostly a matter of attention-value, the intelli-
gence of the fish not being up to par with its sensations.

Bauer's animals were, it is to be noted, thoroughly light-adapted. Dark-
adapted specimens showed no red-shyness, and would freely enter red or
orange illuminations (^620-630m|l) which, when they were light-adapted,
would frighten them over to the dark side of the choice-box. No sudi be-
havior was noted toward any intensities of white light except very high
ones. Far from being blind to red as Hess claimed, the animals perceived
it very vividly according to Bauer. When dark-adapted, they preferred red
to a blue which Bauer considered to be of the same intensity. Therefore,
he thought, the chroma disappeared from the red wavelengths sooner
than it would for the dark-adapted or dark-adapting human. Both a
photochromatic interval for red, and a Purkinje phenomenon, seemed
to have been established for the species.

When spectral lights were used, the fishes did not prefer the yellow-
green as Hess had claimed, but went to either yellow or blue-green. It is
interesting to note that the photopic human has a secondary maximum
of brightness in the blue region (unless the macular pigment happens to
be excessive) . The two maxima are perhaps more nearly equal in bright-
ness for Bauer's species.

When the wavelength of a spectral light was moved gradually up from
the violet end, the fishes first made definitely negative responses at A,510-
m[l, and under a red filter (^680-710m|l) they would scatter into dark
comers if light-adapted, gather under the filter only if dark-adapted so
that its redness was not apparent to them. This seems further evidence
for a photochromatic interval for red (which does not occur in man) ,
though no one seems to have pointed it out.

Mugil, being positively phototropic and lacking in red-shyness, lent
itself to certain experiments impossible or inconvenient with the other
species. Bauer paired a green light with a blue one and regulated their
intensities so that the fishes gathered in the green. When both lights
were reduced equally in intensity the animals shifted over into the blue

478 ADAPTATIONS TO PHOTIC QUALITY

light, thus further demonstrating, to Bauer's satisfaction, a Purkinje
phenomenon.

Box salpa preferred light coming through blue glass + frosted glass to
that transmitted by frosted glass alone. Bauer concluded that this
response was to hue as such, since the blue light was certainly the dim-
mer of the two and Box salpa is strongly positive to light. If it were
responding to brightness rather than to color, the fish would surely have
gone to the white light instead of to the blue.

Hess came forward with an explanation of Bauer's apparent demon-
stration of a Purkinje phenomenon in fishes. He argued that in the light-
adapted fish the expanded retinal pigment would constitute a yellow
filter, reducing the brightness of blue stimuli relative to long-wave ones.
He found that a blue light had to be made four times as intense to bal-
ance a yellowish-red light for a photopic fish as for a scotopic one, and in
experiments with light-adapted tiny carp he had to raise the intensity of
a blue light six- or eight-fold to keep the fishes evenly distributed through
it and a red which balanced the lower blue for the dark-adapted fish.

While no more conclusive-looking demonstration of the Purkinje
phenomenon has ever been made, Hess concluded that it was not that
dark-adaptation increased the brightness of blue and decreased the bright-
ness of red — the true Purkinje phenomenon — but rather that light-adap-
tation left the brightness of long-wave stimuli unchanged and pulled
down the brightness of short-wave ones. Some such effect may indeed
occur along with the Purkinje changes, if the retinal fuscin actually does
have any peak of absorption at all (which has yet to be demonstrated) ,
and moreover has it in the short-wave end of the spectrum. But any such
phenomenon is rendered very improbable by the recent demonstration
that blue and red values are not altered for dark-adapted fishes whose
retinal pigment has been artificially expanded with adrenalin (v. i.).

Hess denied the existence of red-shyness, or at least that it indicated
color-vision; but he failed to look for it in specimens which would be
most likely to show it — mature, light-adapted fish of negatively photo-
tropic species. His finding that red and blue lights could be so balanced
that a light-adapted fish would show no preference for either — even sup-
posing that others had found the same thing, which they have not —
might only mean that the fish had had opportunity to become accustomed
to the red and recover from its red-shyness; he does not give the time-
periods involved. Where Hess finds that a fish will leave a blue and go
to a bright red, he may have been dealing with a red-loving fish — he does

COLOR VISION IN FISHES 479

not mention the species by name. And, where he finds that the fishes
scatter when the spectrum thrown upon them is progressively narrowed
down to red alone, it might only mean that the animals were avoiding
the red because it was such a strong stimulus to them and they were left
with no other light in which to congregate. Hess believed, on the other
hand, that in reduced illuminations blue lights became too strong for the
fish owing to the retraction of the retinal pigment, and in this way ex-
plained Bauer's results with red-blue pairs, wherein the fish would enter
the red light only when the intensities of both were lowered. For Bauer,
this meant that since the fish had become dark-adapted it could no longer
discriminate hues, and consequently had no redness to avoid; but to
Hess it indicated that the blue light had become unpleasantly bright, and
was seen achromatically just as in light-adaptation, but with far greater
brilliance because of the removal of the shielding pigment from its
pathway.

It is interesting to note that in fishes the migration of the pigment
itself, and of the cones, has recently been shown to take place maximally
in yellow light when physical intensities are equated. Red and blue evoke
the least movement of the elements, with orange, yellow-green, and blue-
green intermediate in effectiveness. This checks with Bauer's demon-
stration of a subjective brightness-maximum in the yellow, and also with
the peak of absorption of the photosensitive substance which von Stud-
nitz claims to have extracted from fish cones.

Von Frisch emphasized two techniques, one of which involved train-
ing the fish to respond positively to one of two stimuli regardless of what
the other one might be, and the other of which made use of the response
of the skin pigment cells to colored backgrounds, which since the work
of Pouchet in 1876 had been known to be mediated through the eyes
(see next section). Frisch's training technique was essentially the one
which he had applied so successfully to the bee, in another controversy
with Hess which lies outside the scope of this treatment. After the fish
had been trained to come to a certain colored tube for food, regardless
of where that tube might be in a series of gray tubes in the aquarium,
he omitted the food (thus controlling olfactory and gustatory cues) and
found that the fishes — 'EUritze' (Phoxinus Icsvis) — always went to the
colored tube though six gray tubes at a time, out of a total of 50 gray
shades ranging from white to black, were presented along with the color.
Since there was no shade of gray which the fishes mistook for the train-
ing color, Frisch concluded that they could discriminate hues.

480 ADAPTATIONS TO PHOTIC QUALITY

In this same way Frisch also determined the discriminability of colors
from each other, and found that the fishes confused red with yellow, but
not blue with green or either blue or green with either red or yellow.
Purple was also sometimes confused with red and yellow, suggesting a
closed color circle which was firmly estabUshed years later for Phoxinus
by other investigators employing spectral lights. In 1923, Burkamp
offered Phoxinus as many as 23 pigmentary grays simultaneously with
a training color, whose position in the mosaic of grays was irregularly
varied, and found that the color was never confused with any gray —
an abundant substantiation of Frisch's earlier work.

Frisch essentially repeated Zolotnitzky's experiments, which Hess had
also repeated (with altered technique and complete failure) . After train-
ing Elhitze on yellow meat, Frisch substituted bits of yellow paper on
gray backgrounds of the same texture, including a shade of gray which
matched the yellow for his own dark-adapted eye. On each gray back-
ground he also fastened bits of other gray papers both lighter and darker
than the yellow. Trained fishes snapped mostly at the yellow bits, un-
trained ones equally at all three. Hess repeated this experiment also,
again altering the technique, and got negative results. His fishes trained
positive to yellow would afterwards snap at blue objects as often as at
yellow ones; but it has been pointed out that he had not kept blue objects
out of the situation during the training, and had made no effort to
prevent any 'blue = food' association at the same time that he was build-
ing up the 'yellow = food' one. Frisch also turned the weapon of retinal
migration back upon Hess, when he eventually demonstrated that the
particular intensity in which Phoxinus ceases to discern the chroma red —
is dark-adapted, in other words — is one in which the photomechanical
changes will run to completion of the dark-adapted pattern (see p. 149).

The response-to-background technique also yielded positive results on
Phoxinus in Frisch's hands; and since he first popularized the method it
has since, on less drab species, yielded even more striking findings than
his own. Phoxinus ordinarily responds to a yellow (or red) background
by becoming yellowish. It has no other capacity for color change; but it
responds to light and dark backgrounds by corresponding lightenings
and darkenings of the skin. Frisch took advantage of the fact that the
change in tone takes place in a few seconds, while several hours are
required for the change in hue to be accomplished. From a finely graded
series of black-gray-white papers, he was able to select a gray to which the
fish made the same brightness-response as to a particular yellow paper.

COLOR VISION IN FISHES 481

By alternating the gray and yellow backgrounds he could thus keep the
fish at a constant brightness of skin pattern. Left on the yellow back-
ground for an hour or more, the fish turned yellowish; but it would
never do this on the matched gray.

Similar results were obtained with Crenilabrus pavo and Trigla corax.
And, when yellow and blue fluids, both so concentrated as to appear
black, were used as backgrounds, Frisch found that gradual dilution
evoked graded brightnesses of skin coloration but an expansion of the
yellow chromatophores occurred only in the case of the yellow solution.
He chose two shades of yellow papers and found a gray which gave the
same brightness-stimulation as the lighter of the yellows. When the skin
of a fish had adapted to the darker yellow, substitution of the gray for
the dark yellow caused an immediate paling of the skin. This demon-
strated that the two yellows differed more in brightness than did the
lighter yellow and the gray. Prolonged exposure to either yellow now
caused a yellowing, which would not take place on the gray, or on green,
blue, or violet backgrounds — on these, the xanthophores contracted.

Freytag shortly repeated some of Frisch's work with Phoxinus and got
negative results. His fishes responded to the shade of the background
but not to the color, even after twenty-four hours. Reeves later rather
lamely suggested that Freytag had not waited long enough for the color
change to take place. It is far more likely that Freytag's specimens simply
came from the wrong river! At about the same time, Haempel and
Kolmer were reporting their work on Phoxinus Icevis and Cottus gobio,
where the only color-mimicry they observed was a reddish response of
Phoxinus to red backgrounds, no reaction being given to gray, or to other
colors. Their specimens had come from a red-bottomed river, the Wiirm.
Years later, in 1920, Schnurmann found that while Munich specimens
behaved just as Frisch had described them, others from Ulmar gave no
color-response to yellow, orange, or red backgrounds.

Another fish which is a favorite with physiologists is our own killifish,
Fundidus heteroclitus; but unfortunately its dermal color-repertoire is as
limited as that of Phoxinus. Connolly placed killifishes on backgrounds
illuminated with spectral lights carefully equated in intensity by ther-
mopile measurements. It took several days for the specimens on red and
yellow grounds to become distinct from those on blue. A more versatile
species was found by Frisch — Crenilabrus roissali, which adapts to red,
green, and blue grounds as well as to yellow ones. To the achromatic
(scotopic) human eye the brightnesses of the backgrounds offered by

482 ADAPTATIONS TO PHOTIC QUALITY

Frisch were in the order yellow->green^blue->red. Since the fish reacted
to the 'brightest' color by contraction, to the 'darkest' color by expansion
of its pigment cells — this being quite unorthodox for pigment cells to do
— Frisch concluded that the reactions were being made to the hues per se.

Critics were quick to point out that while these reactions admittedly
might be made to the hue of the background, and mediated through the
eyes (several investigators had been so thorough as to make sure that
that blinded fishes could not make them) , there was still no reason to
assume that the fish must therefore be consciously aware of the hues.
These objectors were largely silenced by the work of two American
investigators, Sumner and Mast.

Sumner, in 1911, had been intrigued by the rapidity of the color
changes of flat-fishes as they glided over the changing bottom. In Rhom-
boidichthys podas, Rhombus Icevis, and Lophopsetta aquosa, he had
demonstrated dermal responses to shade, color, and pattern. These
species reacted to black, brown, and gray, but not to red or yellow.
A few years later Mast published his classical studies on two other
genera, Paralichthys and Ancyclopsetta, which in a startling way mimic
blue, green, yellow, orange, pink, and brown. Shade, color, and pattern
are all closely followed by the dermal adaptations.

Mast painted the floors of a number of tanks, some with a single color
and others with two colors on the respective halves. He allowed flounders
to remain on single colors for six weeks, then placed each fish on the
dividing line of a bicolor tank floor. Blue-adapted fish swam at once to
the blue side of a two-color tank 88% of the time, green-adapted fish
70% to the green side. But red-adapted individuals turned toward the
red only 26% of the time. If their choice had been a 50:50 one, Mast
contended, it would have meant that they could not discriminate the red
hue from the other. 26% meant actual avoidance of red. When the other
side of the tank happened to be blue, red-adapted flounders went to the
red side only five times, to the blue 115 times!

The responses of Mast's flounders were so immediate, so obviously
visual, that they were far more important than the Phoxinus work as
grist to the mill of the proponents of piscine hue-discrimination. But
brightness was not controlled, nor was a series of confusion-grays em-
ployed in Mast's experiments. They demonstrated color-discrimination,
but did they show /?Me-discrimination? By this time most of those inter-
ested were convinced either that Hess or Frisch was right; but some
remained unsatisfied with the results and the limitations of colored-

COLOR VISION IN FISHES 483

paper techniques. Sporadic investigation continued, with training meth-
ods and filtered or spectral lights emphasized more and more.

Goldsmith came to the support of Frisch with a report on Gobius
fluviatilis and Gasterosteus aculeatus. The former of these species was
red-shy, the latter red-loving, as were also some young plaice which she
tested. Goldsmith's experimental results were practically worthless, for
in an attempt to prove hue-discrimination she fell into the brightness
trap in a new way : where so many others had assumed that equal bright-
nesses for the human would be equal for the fish, Goldsmith assumed
that equal energies would be equally bright. That idea was alright for
its time ; but she proceeded to equate the energies of her lights by adjust-
ing their intensities until they darkened photographic plates to the same
extent in the same exposure time. The visible spectrum of any camera
film is of course very different from that of any eye. With such stimuli,
Goldsmith established that Gasterosteus preferred red>yellow>green->
blue, and concluded that the choices were made on a basis of hue. Her
one permanent contribution was in finding that a fish trained to come for
food to colored forceps would persist in examining empty forceps bearing
the training color for as long as four days after a previous test.

No new reports appeared until just after World War I, when those
of White and Reeves — the latter perhaps the most important single con-
tribution to date — were published. White worked on Umbra limi and
Eucalia inconstans, using pigmentary colors. She found that grays and
white lights were scarcely discriminated as to intensity, and that after
training to one of two colors neither species could be confused by any
intensity of the negative stimulus. Umbra discriminated between red and
green, red and blue, and yellow and green. Eucalia could discriminate
red from green, but not blue from yellow. White's steps in albedo were
coarse, but she reasoned that since the discrimination of intensity was
so poor there was no need of seeking any more perfect match in bright-
ness than the fish was able to make. Criticized on this ground, she re-
peated her work (as Hineline, 1927) but with a technique actually
inferior to her original one. Misled like Goldsmith by a prevalent notion
that equal energies should arouse equal subjective brightnesses in any
and all animals, she obtained filters equated within a few per cent in
total visible energy transmitted. With these, she found that Umbra was
able to discriminate red (?i660-700m^) from green (A,510-550m[l), red
from blue (X400-450m[i) , red from yellow (A,560-600m(l) and (with
difficulty) yellow from blue, but could probably not distinguish blue

484 ADAPTATIONS TO PHOTIC QUALITY

from green (A510-550m[x). One member of each pair was the positive
stimulus at first, and the fish was later retrained to the other stimulus —
a further attempt to eliminate preferences or any possible discrimination
on a brightness basis.

White-Hineline's decidedly inconclusive work was far overshadowed
by the restricted but thorough and beautifully controlled investigations
of Reeves, a student of Reighard. Reeves was content to employ two
hues only, devoting her time and energy entirely to the elimination of
the brightness factor from this one discrimination. While other more
recent researches have yielded superficial information about much more
of the whole color-vision system of the fish, that of Reeves stands as a
model demonstration of an unquestionable discrimination of hue as hue.

She used an adaptation of the Yerkes- Watson discrimination box
described in the 'ideal investigation' outlined above, and studied the
untrained and trained responses of several species, chiefly Semotilus
atromaculatus and Lepomis gibbosus, to white and (filtered) red and
blue lights. The blue filter passed the short-wave end of the spectrum
up to ^509m(l. Several different red filters were used, principally one
which transmitted only wavelengths longer than 589m[l.

The dace (Semotilus) showed very poor brightness-discrimination in
preliminary experiments. At least they would not distinguish intensities
which differed in less than 1 :4 ratio. When two such intensities were
presented, apparently barely discriminable by the animal, the insertion of
the red filter in the path of the brighter light (without any other change
being made) produced a marked change in behavior, although the
intensities were presumably no longer discriminable, being too nearly
equal. The fish evinced a strong red-shyness, which however was tempor-
ary and in young individuals was absent. Dace were now trained positive
to a dim blue stimulus versus an intense red one. After training, the
intensity of the red was cut to 60%, 37%, then 20% of its original
value, the dace still going to the blue to seek food 90% of the time.
Repeated with more gradual reduction, the typical response was an 85%-
95% correct choice until a critical value of red intensity was reached,
at which the accuracy suddenly dropped to 60%!

At this point, the two stimuli were obviously alike in some way for
the fish. A permanent performance of 50% or 60% accuracy would have
meant that they were wholly identical; but Reeves found that with no
further changes the accuracy eventually rose again to 83%, and upon
a still further dimming of the negative stimulus the performance went

COLOR VISION IN FISHES 485

still higher and remained high. She felt justified in concluding that the
intensity of red at which confusion at first occurred was one at which
the brightnesses of the red and blue lights were equated for the dace,
and that the confusion was due to a re-learning, the fish switching its
attention from the brightnesses to the hues and making the association
'blue = food' which she had supposed to have been made in the first
place. Another dace showed no such temporary confusion at any inten-
sity of the red, indicating that it had been attending to hue from the
first, rather than to brightness. Of course there were two other possi-
bilities— that the fish, from the outset, were not going to blue so much
as avoiding red, with individual differences in this red-avoidance; or,
that the confusion was due to getting used to red and ceasing to avoid it,
the 'blue = food' association being not yet established. But, interpreted
in any of these ways, the experiment had demonstrated hue-discrimin-
ation, for there could be no redness-fear in the first place unless there
were redness-perception.

The sunfish (Lepomis) proved to be more sensitive to intensity than
the dace, tending to lurk and hide in dark corners rather than come out
and face white lights to which the dace had readily gone. In keeping
with this. Reeves found a greater capacity for discriminating intensities,
the ratio needing to be but 1 : 2+, which however was still far short of
the 1 : 1.23 difference claimed by Hess — and yet was far better than the
capacity elicited from any other species by any other investigator before
or since. When offered blue versus red, the sunfish was extremely slow
to build up the 'blue = food' association; and again it was the larger
specimen which showed red-shyness, the younger specimen lacking fear
of red as also of many other things which would startle the older animal.
After successful training positive to blue, the gradual dimming of the
red stimulus to a certain value caused the same sudden confusion, at
that critical intensity, which had been manifested by the dace — the
intensity this time being, by coincidence certainly, the very one at which
the red and blue were identical to Reeves' own dark-adapted eye (the
fishes were Ugh t-a.dsipted by an initial white illumination before each
trial). The sunfish recovered from the confusion at matched bright-
nesses much quicker than had the dace, however. Both species readily
discriminated the training-blue from 'gray' light (produced with several
layers of photographic negatives as a filter) which matched it in bright-
ness for the human; but they behaved very differently from what they
did when a blue and a red, also of equal brightness to the human, were

486 ADAPTATIONS TO PHOTIC QUALITY

simultaneously offered. Reeves drew the natural conclusion that the fishes
saw the red and the gray as qualitatively different things, since the two
equalled the same thing (the blue) for the human in brightness. There
is an obvious fallacy here, but it is of no importance to the main con-
clusion that hue discrimination occurs in the two species.

Both species were much more sensitive to lights when dark-adapted,
but Reeves could find no evidence that there was any change in the
relative brightness of red and blue or of red and white. She therefore
questioned the occurrence of a Purkinje phenomenon, though on quite
different grounds from those of Hess. The importance of the presence
or absence, or demonstrability, of a Purkinje shift for the certainty of
hue discrimination has been greatly overemphasized as explained above
(pp. 474-5).

Reeves came close to the conditioned reflex technique — a very modem
tool of research on animal color-vision — in her observations on untrained
mud-minnows (Umbra litni) and shiners (Notropis cornutus). She
noticed that the respiratory rate of mud-minnows was the same (30/
min.) in daylight, and in daylight plus tungsten-lamp illumination.
When she slipped a ruby glass plate under the lamp the fishes settled
to the bottom, had fits of trembling, and more than doubled their
breathing rate. Shiners breathed 60 times per minute in diffuse daylight,
85 times per minute when a carbon filament lamp was turned on in
addition, and 150 times per minute when a ruby filter was placed over
the lamp. In this experiment it was perfectly clear that the response was
to redness as such, since the respiration rose with an increase of bright-
ness, but rose still higher when that brightness was somewhat reduced
by a filter which introduced hue.

Untrained Hyborhynchus notatus would readily approach blue and
gray patches of light equated in brightness for humans and offered side
by side. But when a red, equated in brightness with the other two stimuli
for the light-adapted human, was substituted for the gray, the minnows
stayed away. Untrained Semotilus behaved identically. When, after the
blue and red had been offered for two hours, the gray was returned in
place of the red, they approached the patches promptly; but the red-
shyness reappeared when, three hours later still, the red was once more
exchanged for the gray. Strangely enough, trained dace were just as shy
of gray as wild ones were of red.

Differential behavior of fishes toward blue, red, and gray matched in
brightness for the human eye, either light- or dark-adapted, is suggestive

COLOR VISION IN FISHES 487

but not conclusive. Here again Reeves improperly assumed that lights
equally bright for one animal would be equally bright for another, which
could be true only if their spectral luminosity curves were completely
superimposable or at least coincided with, or crossed, each other at the
particular wavelengths used.

Since Reeves' time, all of the training experiments reported have been
made on Phoxinus Icevis and, to some extent, on Gasterosteus aculeatus.
Schiemenz, Wolff, Ktihn, and Hamburger, working from 1924 to 1926,
are the last prominent names in the literature to date. Spectral lights
were used ahnost exclusively, and the spectrum of the fish explored with
sufficient thoroughness to establish its limits roughly and to yield curves
of hue-discrimination — that is, graphs of the closeness of two just-
discriminable wavelengths plotted against their position in the spectrum.

Light-adapted fishes were trained to jump for food held just above
the water on glass rods bathed with narrow spectral bands. They would
continue to seek food on empty rods in the training color even when
twelve intensities of it were interchanged at random, and were never
confused by any intensity of any other color except the training color's
immediate neighbors in the color circle. Lights too low in intensity to
be seen as colored by the human were the only ones confused by the fish.
Trained to seek food in a particular colored area among others — a
multiple version of Reeves' two-choice presentation — they were never
confused by the other colors regardless of intensity-relationships. These
species apparently give much more attention to hues than to brightnesses,
in contrast to Reeves' material.

The animals' ability to discriminate hues close together in the spec-
trum was better in the short-wave end, a little poorer in the long-wave
region, than that of man. They could be trained to ultraviolet as far
as A,365m[X; and this region, violet, blue, green, yellow, and red were all
qualitatively different for the fish. When offered the whole spectrum
on the wall of the aquarium, they gathered in the particular region to
which they had been trained, and snapped the air seeking the accustomed
food. If the spectrum was moved, the fishes shifted with it. If the in-
tensity of the whole spectrum was lowered they still gathered in the
training color as long as it had color for the human, despite repeated
scattering by hand and shifts of the position of the spectrum. And they
could not be trained at all to particular brightnesses of white light.

These high-school EUritze thoroughly dispose of Hess's contention
that all fish are color-blind. Although the English worker, Bull, has very

488 ADAPTATIONS TO PHOTIC QUALITY

recently brought the conditioned-reflex method to bear upon the question
of hue-discrimination in fishes, his revelation of the ease and speed with
which simple discrimination can thus be proven, as compared with the
training method, has come too late to save any investigator's time or
trouble. Bull's methods cannot rival the training technique for the labor-
ious working-out of a color-vision system, and it is this that remains to
be done. No reasonable student of the problem any longer doubts that
fishes — all duplex teleosts at least — can experience hue as a sensation-
quality apart from brightness.

The 1924-1926 work discussed above has revealed some preliminary
data on the nature of the hue system of Phoxinus, which has such a head
start that probably no American species will be worked out sooner.
Hungry, partly trained individuals have been found to snap for food in
bands of wavelengths neighboring the ones used for training. Thus, red-
trained animals will snap also at yellow while still incompletely trained,
yellow-trained ones snap also at red and green, 'blue' animals at green
and violet. Some of these confusions persist after thorough training,
enabling the determination of a curve of hue-discrimination which is
interestingly different from the human one, and has seeming maxima at
MSOm^l, A,485m[X, A,590m[l, and probably at X655m[l. The human is
nowadays believed to have but two genuine maxima, at 7,490m[A and
7,580m|l, though from one to three other secondary maxima were
described by the older investigators. Probably some of the 'maxima' of
Phoxinus will disappear in future investigations.

A valuable finding upon imperfectly trained Ellritze was that those
undergoing training to red made most of their erroneous snaps in the
violet and ultraviolet, and vice versa. This demonstrates a recurrence of
redness in the short-wave sensations, closing the color circle through the
red-blue and red-violet mixtures which the human sees as the extra-
spectral purples. It would be most interesting to know, though sadly
unknowable, whether ultraviolet is 'red' to fishes that can see it, or would
look red to us if our optic media did not fluoresce it so completely into
pallid short-wave visible light. For many fishes, the penetrability of the
ocular media ceases in the (human) violet; but in Gasterosteus aculeatus,
for example, the wavelength 313m[X can reach the retina. Merker, the
leading investigator of the biology of the ultraviolet, notes that these
sticklebacks can be trained to snap for food in the wavelength band
313-253m[l, but thinks that in such very low wavelengths the food is
seen as a shadow cast by visible light into which the fluorescence of the

COLOR VISION IN FISHES 489

water converts the extreme ultraviolet. The fixing of the short-wave limit
of the true visible spectrum for such an animal is very difficult. In Gaster-
osteus, in contrast to the frog, no retinal action-current can be detected
in ultraviolet illuminations; and yet a pure ?l366m[i beam, apparently
visible to the fish, causes the complete pattern of retinal photomechanical
changes. Quinine-fluoresced light will do likewise, however. Through
fluorescence, ultraviolet light may paradoxically lead to seeing without
actually itself being seen. The exact position of this lower spectral limit
for fishes in general is of little or no biological importance anyway, for
a meter or less of water eliminates all of the ultraviolet in sunlight.

Something, then, is known of the spectral limits, hue-categories, and
hue-discrimination in different spectral regions for these two fishes, and
we can hope eventually to learn all about the system they employ —
whether it has three component central processes, or more. We can
already be certain that they are not dichromatic, for they distinguish too
many hues and, according to Hamburger, get no sensation of 'white'
from any monochromatic light, and therefore have no neutral point.
Hamburger made a beginning at an analysis of the laws of color mix-
ture as they apply to Phoxinus. He found that fishes trained to white
light not only discriminated it qualitatively from every spectral region
but recognized, as white, human complementary mixtures of yellow and
blue, red and blue-green, orange and blue-violet, and so on. A similar
demonstration of complementary colors for Betta splendens, by an en-
tirely different technique, was incidental also to the work of Beniuc
(see pp. 364-5).

It is one thing to be able to say that all cone-rich teleosts assuredly
have color vision, and quite another thing to say how much color means
to fishes. The environment of the average species is rather drab. We
have seen that particular colors — red and blue — may provoke particular
species to vigorous responses. Miss Reeves' fishes tended, however, to
pay more attention to brightness than to hue. How successfully might
form also compete with color for the attention of a fish? Is the shape of
an artificial lure perhaps more important than its color, even though the
latter is perceived? Recently some experiments have been made along
this line by a Japanese, Horio :

This investigator trained carp positive to a red disc and negative to a
blue one. They learned this discrimination readily — not so readily, how-
ever, the discrimination of a white triangle (positive) and a white square
(negative) . The better to compare the effectiveness of form and color,

490 ADAPTATIONS TO PHOTIC QUALIT^

Horio then sought a pair of colors which would be as difficult for the
fish to tell apart as were the triangle and square. He found it, in violet
and blue. Trained positive to a violet disc versus a blue one and to a
white triangle versus a white square, then offered a violet square versus
a blue triangle, the fish went to the positive color rather than to the
positive form. Color thus seems to lie between brightness and form as
regards its attention value.

When color and form were used in summation instead of at cross-
purposes, Horio obtained some unexpected results. Fishes partially
trained to a red or violet disc versus a blue one, and separately to a
white triangle versus a white square, made more accurate choices when
offered a red or violet triangle versus a blue square than when the
stimuli differed in only color or form. But when these independent
trainings to color and form were both complete, the fishes made more
errors on the combination stimuli than on the simple ones. Horio de-
cided that this must mean that the fishes had had time to develop 'red
disc = food' and 'white square = no food' associations, not merely 'red =
food' and 'square = no food' ones. Hence, the red triangle had a weaker
effect on them than either the red disc or the white triangle.

Amphibians — Most of the Amphibia are nocturnal and secretive, and
it is difficult to see what color vision could do for them if they had it.
The common (ranid) frogs are arhythmic animals however, which might
have, and might benefit from, color vision. Except for one recent
Japanese report of work on a larval salamander, which the writer has
not been able to see, all of the efforts to find color vision in amphibians
have been made upon frogs.

As early as 1900 it was established by Himstedt and Nagel that the
frog has a Purkinje phenomenon. Their technical tool was the electro-
retinogram, the record of retinal action-currents. Granit and his co-
workers, with similar but refined methods, have found the photopic and
scotopic maximally-effective wavelengths to be practically the same
(560mp, and 507m^) as those giving the peak brightnesses for the
human. Therman, in the same laboratory, found an increased electrical
response in blue light and a decreased response to red, in dark-adapt-
ation. Expansion of the retinal pigment in darkness by injections of
adrenalin failed to upset this relationship, casting further doubt — if any
were needed — upon Hess's interpretation of the Purkinje phenomenon
in fishes.

COLOR VISION IN AMPHIBIANS 491

The presence of a Purkinje phenomenon, however, is no evidence for
color vision, but only demonstrates the presence of two types of receptors
with different absorption spectra. A Purkinje phenomenon of the iso-
chromatic type could exist in an animal with a duplex retina and achrom-
atic vision. Hess even denied the existence of the phenomenon in the
frog, on the basis of pupilloscopic findings, claiming the frog pupil to
be most responsive to green light both scotopically and photopically.
We have seen how devoid of any certain meaning such findings are,
particularly when gained in an animal whose iris muscles are wholly
or largely autonomous. Pupillometry is scarcely more trustworthy as a
means of determining accurately the limits of the spectrum; but it is
a convenient means, and with it Hess determined the spectral limits of
the frog and other amphibians to be practically the same as those of man.

Nearly forty years ago, Yerkes studied the learning ability of the
green frog (Rana clamitans) in very simple mazes, employing red and
white cards as parts of the stimulus patterns offered the animal as cues
to true path and blind alley. The frogs were guided partly by these
grossly different visual stimuli; but neither Yerkes nor anyone else has
since gone further than this in attempts to train frogs to discriminate
hues. Their learning ability, which is next door to zero, makes this quite
out of the question. Hess and others got nowhere with the color-pref-
erence method in frogs; and even the conditioned-reflex technique,
which obviates any need of a conscious choice by the animal, gave no
results when Bajandurow and Pegel tried to apply it to the frog in 1932.

Promising leads have come lately from the electroretinograms picked
up from the excised eye under monochromatic stimulations. The Helsinki
group found that the form of the gram is different for colored stimuli,
when differences in intensity are ruled out. They have decided that there
must be three systems in the frog eye :

A. The rods, with their rhodopsin.

B. Rods, or cones, containing a substance absorbing light maximally
in the blue and violet ('green rods' [p. 58]? cone oil-droplets?) .

C. Cones of at least two types (the singles and doubles?) overlapping
with respect to the distribution of their sensitivities to spectral lights.

They conclude that "the selective effect of wavelength on the retina
represents a mechanism that can be used for color differentiation." But
when they plotted the spectral distribution of the effects of strong mono-
chromatic lights upon the subsequent electrical response to stimulations

492 ADAPTATIONS TO PHOTIC QUALITY

with a standard A,500(J, source, they obtained a curve which coincided
neither with the rod-spectrum nor with the cone-spectrum as deduced
from the ordinary electroretinogram — nor with a curve representing the
superposition or resultant of the two. This is rather indigestible, and it
is to be hoped that these workers (now estabhshed in Stockholm) may
soon decide to turn their recording apparatus upon some animal —
Phoxinus for example — which is known to have color vision and whose
system is susceptible of cognate studies with various other procedures.

The only investigator who, without 'hedging', makes an out-and-out
claim of color vision for the frog is Birukow. In 1939 he reported experi-
ments based upon an application of the optomotor reaction (pp. 301-2) :
In 1927, Schlieper had reported that when the alternate stripes on the
revolving drum used for eliciting compensatory movements from the
animal inside it were respectively colored and gray, there was always
some shade of gray to be found which, paired with a given color, would
evoke no response from the animal. The animal behaved as though the
visual field had become homogeneous, its motion invisible to him — in
other words, the animal acted as if it were color-blind, even though it be-
longed to a species known positively to have color vision. Schlieper used
several diurnal insects, two fishes, and the lizard Lacerta vivipara. By all
of these, the optomotor reaction was apparently given only to patterns of
brightness differences, and Schlieper concluded that the critical shade of
gray which, paired with a color, brought no response, must be a bright-
ness match for that color.

Von Buddenbrock and Friedrich, a few years later, reasoned that if
two colors were adjusted in brightness so that each by itself matched the
same gray, the two colors would then be equal in brightness for the
animal. Such matched colors, applied in alternate stripes to a drum, did
effectively stimulate their animals to make compensatory eye movements.
Unfortunately, they employed this technique only with invertebrate
material — a species of crab.

Birukow was the first to use their procedure on vertebrates, and he
chose to study Rana temporaria. At least, he assumed that Buddenbrock
and Friedrich's ideas were correct, and was prepared to try them out on
the frog. But he found that neither red nor blue could be 'matched' by a
gray for this animal. Apparently the frog differed from the lizard in
some way; and the failure to find a gray which, alternated with a color,
suppressed the reaction, proved the perception of the color. Birukow
could offer no explanation of Schlieper's results with the lizard, nor

COLOR VISION IN AMPHIBIANS 493

could he very well apply Buddenbrock and Friedrich's principle of pair-
ing off colors that matched the same gray. He did find that yellow-green
and its spectral neighbors could be equated to grays, and decided that in
the case of the frog (in contrast to the lizard) this meant that they were
gray to the animal, yellow-green thus being a neutral point in his spec-
trum. At intensities below .04 lux, any color could be equated to a gray
— this being the realm of pure rod activity, A marked Purkinje phenom-
enon was found, but above 30 lux there were no further changes in the
relative brightnesses of different colors. When the drum was striped with
alternate red and blue, and the stripes made progressively narrower, the
reaction was inhibited when the visual angles subtended by the stripes
were twice the threshold values for black and white stripes. Birukow con-
cluded that the 'visual acuity for colors' was only half of that for black
and white. Ignoring the fact that the differences in albedo of the adjacent
stripes were far from the same in the two cases, he correlated these find-
ings with the fact that the cone-to-rod ratio in the frog's area centralis is
1 :2. Again, ignoring the fact that while rods may play no part in color
vision, cones do play a part in black-and-white vision, he related his find-
ings to the fact (earlier demonstrated by himself) that it is the rods
rather than the cones which, in the frog, set the retinal limits of resolving
power. From all this he drew confirmation that the rods play no part in
color vision.

The use of the optomotor reaction as a means of studying animal
visual acuity has been severely criticized. Apart from this however, does
the frog's compensatory reaction to red and blue versus gray stripes of
any and all albedos prove color vision? There is grave doubt of it. The
average investigator, finding that he could obtain a yellow-gray match
that abolished the reaction, would certainly not give up on red-gray com-
binations until he had tried many close grades of gray. And as a matter of
fact, a close perusual of Birukow's report reveals that his animals did have
matches of gray and blue, despite his conclusion drawn to the contrary.

Again, the reaction to blue versus red of any and all albedos could
have a purely physical basis. Considering such factors as chromatic aber-
ration, it is hard to imagine how the parade of contours between the red
and blue stripes could be made to disappear even for a totally color-blind
animal for whom the red and blue were exactly matched in brightness.
The optomotor reaction is no more reliable as a means of studying color
vision than for tests of visual acuity.

494 ADAPTATIONS TO PHOTIC QUALITY

To sum up Birukow's work : He has not demonstrated that the frog
necessarily has any reactivity to hue. If his animals were responding to
hue by such a pure reflex as the optomotor reaction, we can tell no more
about whether they have hue sensations, by means of Birukow's proce-
dure, than we could with a conditioned-reflex technique. If we even
assume that Birukow's conclusions are justified (correcting the one
regarding blue) then we must believe that the frog has a 'red' sensation,
but no hue sensations from medium and short wavelengths — his neutral
point is really a neutral region, which nearly fills his spectrum. But if the
animal does also see blue as Birukow claims, then the frog stands reveal-
ed as the only known vertebrate whose color-vision system is dichromatic
and has a neutral region instead of a neutral point. Until much better
evidence than Birukow's is produced, we had best conclude tentatively
that the Amphibia have no color vision whatever.

Reptiles — Aside from the age-old supposition that the chameleons can
change color to suit any and all backgrounds, and do so because they
see the colors of the backgrounds, the writer has been able to unearth
only one statement about reptilian colorvision from the dark ages of
comparative psychology. It was made regarding the common European
turtle (Emys orbicularis) by an old-time French naturalist. He found
that when this carnivorous species is offered a rose leaf, it will ignore it
and try to seize the proffering finger; but when offered a rose petal the
turtle grasps it at once "because it is the color of a piece of raw meat."
This sort of experiment is interesting, but no more than that; and a large
portion of its interest lies in the belief inherent in the investigator, and
so widespread among laymen, that if any animal can distinguish any
hues it should at least be able to recognize those of foliage and blood —
the two most important colors for herbivores and carnivores. It seems
almost illogical that the hues yellow and blue should be so favored by
psychologists as the 'most primitive' colors in hypothetical phylogenetic
schemes of human color vision!

Not until recently was any real investigation of reptilian color vision
made, apart from the inevitable pupilloscopic studies and food-visibility
experiments of Hess, which showed a shortening of the short-wave end
of the spectrum, as in diurnal birds. In 1933, Wojtusiak published his
work on a turtle, Clemmys c as pic a, in which a training technique was
used, with colored papers and colored lights as stimuli. As with the fishes,
intensity-discrimination appeared to be remarkably poor — the turtles

COLOR VISION IN REPTILES 495

could be trained to distinguish grays only if their shades were very differ-
ent; but they distinguished each of several colored papers from any of
seventeen grays.

Twelve spectral lights were discriminated qualitatively, and the indi-
cations were that with longer training a great many more hue differences
might have been shown to occur for the species. The trained human
observer can distinguish about 160. The spectral limits for the turtle
were at least as low as 7,401m^ and as high as X760m\l — much the same
as for man and most other vertebrates. Hues were most easily told apart
when in the neighborhood of orange-red (A,634m|x), with weaker max-
ima of discriminability at the blue-green (A504m[l) and violet, and a
minimum in the blue.

The most important hues for the turtle appeared to be orange, green,
and violet. Yellow and yellow-green, when not accurately discriminated,
were apparently most often seen as orange; but red was separated from
the general orange category and seemed to be more akin to violet for the
animal, which thus has a closed color circle. These peculiarities were
attributed, probably quite properly, to the restrictive filtering action of
the meager assortment of oil-droplet colors possessed by the turtle (see
Chapter 8, section D) . In contrast to the fishes, and in keeping with the
predominantly red and orange oil-droplets, the turtle showed an elevated
capacity for hue-discrimination in the long-wave region, where also the
position of the photopic brightness maximum was shifted from its human
(yellow-green) value well into the orange, toward the red. This incident-
ally is not in keeping with the properties of the turtle's 'zapfensubstanz'
(maximum absorption at A,560m[x) as given by Studnitz. The oil-droplets
also account for the observed low ability to discriminate hues in the
green and especially the blue region, but the apparent slight rise found
in the violet region seems paradoxical.

Wagner, a year before Wojtusiak, and working in the same laboratory,
published the only study to date on lizards, apart from the peculiar
results of Schlieper on Lacerta vivipara mentioned above. His technique
was simple but effective. He found that Lacerta agilis was violently dis-
gusted by the taste of salt. Offering meal-worms pinned in front of discs
of colored paper on long handles, he obtained rapid training positive to
normal worms presented with one stimulus and negative to brine-soaked
ones offered with an alternative stimulus. When each discrimination was
finally established, as evidenced by twenty successive correct choices.

496 ADAPTATIONS TO PHOTIC QUALITY

Wagner gave the lizard ten additional control trials with both meal-
worms palatable, thus eliminating any discrimination on the basis of
taste, smell, or differential behavior on the part of the salted and un-
salted worms themselves.

The most surprising discovery was that it was impossible to train the
lizards negative to green. Their preference for this, the most common
color in their natural environment, was so strong that when four colored
discs bearing palatable food were offered simultaneously, the numbers of
times they were approached were: green, 95; yellow, 79; red, 67; blue,
59. When four very different Hering gray papers (numbers 2, 7, 11, 15)
were similarly presented, the animals showed no preference for any.

When for twenty successive trials gray, white, or black was offered
along with colors on a handle holding four discs, approaches to the
respective stimuli were as follows in three such series of trials :

I. Gray, 14; green, 5; red, 1; blue, 0.

II. White 11; green, 5; blue, 2; black, 2.

III. Yellow, 9; red, 5; blue, 4; black, 2.

Thus, gray was preferred to colors — even to green — and white was pre-
ferred as if having a value of light gray. Black seemed to have the value
of a color, next to blue (which would presumably be seen very darkly,
through the yellow oil-droplets present).

Stimuli were thus valued by Lacerta agilis in two groups : (a) white,
grays of all medium shades, and green; (b) yellow, red, blue, and black.
Group V was strongly pi:eferred to group 'b\

With pairs of stimuli, Wagner obtained discriminations of red, orange,
yellow, yellow-green, ice-blue, deep blue, and violet from each other and
from any of seventeen grays. In keeping with the presence of only yellow
oil-droplets (though Wagner, apparently misled by the situation in his
colleague Wojtusiak's turtles, speaks of red ones also), hue-discrim-
ination seemed to be maximal in the red and blue, minimal in the green.
These determinations were crude and of course only tentative, awaiting
further work by some investigator using a greater variety of stimuli,
preferably in the form of spectral lights.

There have been no reports bearing upon color vision in crocodilians,
except negative pupilloscopic ones. We know only that the spectral limits
of crocodilians correspond with those of mammals; and, from Laurens'
work, that the alligator has a Purkinje shift from a scotopic maximum of
?L514m[X to a photopic one at X544m|i.

COLOR VISION IN REPTILES, BIRDS 497

A majority of snakes are pure-cone, but the strange history which their
eyes seem to have had (see Chapter 16, section D) makes it anything but
presumptive that they have retained the color vision of their lizard an-
cestors. If they have color vision, it is de novo; but it is unlikely that they
do, since their cones are plump (Fig. 26a, p. 63) and their vision, in con-
sequence, is crude and unsharp as compared with other diurnal verte-
brates. Experimental evidence is wanting, though Kahmann several years
ago mentioned that his training of 'an exceptionally trainable snake
species' to red and blue had succeeded quite well. He has apparently
published no full account of this work.

Of all the unstudied reptiles, it is the geckoes and Sphenodon which
offer the greatest interest. There is a large 'hole' in the Duplicity Theory,
which can be plugged only when we know whether such forms have
retained the color-vision machinery of their diurnal ancestors despite
their transmutation of cones into functional rods.

Birds — No one has ever scientifically questioned that the diurnal birds
have color vision. Since 1863, when Krause first interpreted the multi-
plex oil-droplet mosaic of birds as a mechanism for hue discrimination
(see pp. 192-3), no doubt of a hue-perceptive capacity on the part of the
birds has ever had a chance to grow.

Though color vision was assumed for decades before it was ever
proven by experimental work, that work has fully justified the assump-
tion. During the last quarter-century the researches on avian color vision
have not had to be wasted in controversy as to whether birds see colors
or not, but have been devoted directly to such matters as the determin-
ation of the spectral limits, the relative brightnesses of colors for the bird,
and the latter's capacity for hue-discrimination in different parts of the
spectrum.

For years it was generally believed that the birds are blind to violet
and blue, the short-wave end of their spectrum greatly shortened. The
work of Hess up to 1912 seemingly established this beyond doubt.
Sprinkling rice grains in a spectrum projected upon a white floor, he
found that fowls would eat the rice from the red end to the junction of
the green and blue, but would peck no grains in the blue or violet lights
— allegedly, because they could not see them. The absorption of short-
wave light in the red and yellow cone oil-droplets was held accountable,
despite the fact that the many colorless cones (and the rods) should have
been able to record blue rice — though perhaps hazily, and not as blue.

498 ADAPTATIONS TO PHOTIC QUALITY

Along with this blue-blindness, a sensitivity to red greater than that of
man seemed also to be demonstrated by this early work.

Between 1916 and 1926, the experiments of Hahn, Honigmann, and
Blasser painted a different picture. By staining rice grains with different
dyes or by illuminating them with colored lights, gluing down the grains
to which it was desired to train the birds negative, they showed that the
domestic hen does see blue and violet, though weakly. She does have a
partial, relative blue-blindness, which increases during growth, presum-
ably because of deepening oil-droplet pigmentations. More important
however is her 'blue-shyness', which must be overcome by patient training
before she is convinced that blue objects can be good to eat — the best
explanation of Hess's results is simply that for a hen, there are no blue
foods in nature!

In the meantime, some very careful work had been done in this coun-
try by Watson and Lashley in 1915 and 1916, but because of the war it
went unnoticed abroad for years. They used superlative apparatus afford-
ing brilliant beams of pure spectral lights. With a training technique,
Watson was able to fix the chick's spectral limits as lying between
A,700m^ and A,715m[i at one end and between A,395m|i, and A,405m[X at
the other. His preliminary experiments upon thresholds for colors indi-
cated that these were about the same as in man, except for the far red to
which the chick was somewhat more sensitive. Similar work with the hom-
ing pigeon revealed spectral limits of A,420m|l and A,712m[i, indicating
that Hess had also been in error in claiming the pigeon to be blind to
blue and violet.

Lashley carried on from here, using essentially the same apparatus and
procedure. He was able to train his game bantam cocks positive to red
(7.650m[x), yellow (X588mp, and A,565mp,), green (A,520m|i) and blue-
green (A,500m^), and to discriminate each of these from other colored
and white lights of any brightness. By changing the wavelength of the
negative stimulus, making it closer and closer to that of the positive one
until discrimination failed, and repeating this procedure in various parts
of the spectrum, he was able to plot a curve of hue-discrimination which
proved to have the same number of maxima, in about the same locations,
as the corresponding graph for man. The hen's color-vision system is cer-
tainly trichromatic, probably essentially identical with our own — though
it was independently evolved (consult Fig. 156, p. 519) ; and the filtering
action of the oil-droplets is of course a modifying factor.

Simultaneous color-contrast has been shown to exist for the hen, just

COLOR VISION IN BIRDS 499

as for ourselves. Revesz, in 1921, trained birds to peck rice from pieces of
green paper on large gray backgrounds. He then offered them rice on
both green-on-gray and gray-on-red combinations. The birds took food
from both, showing the 'induction' of greenishness, in the gray, by the
surround of complementary red. When offered gray-on-gray, or gray on
colors other than red, they were negative. By a similar procedure, blue-
yellow contrast phenomena were also elicited.

Few species other than the convenient domestic fowl have been studied
to any great extent. Hamilton and Coleman investigated the hue-discrim-
ination curve of the pigeon in 1933. They used a procedure quite differ-
ent from Lashley's, altering the wavelength of the positive stimulus, by
lOmfJ, steps, toward that of the negative stimulus. The wavelengths near
which small differences in hue were best appreciated proved to be 580m|l
and 500m[X — values not far from those for man (580m|i and 490m|x) .
The indications were that in the pigeon the 'green-ness' process (p.
94) does not commence until ?L620m[j, is reached, instead of at 650m[X
as in man; and at X530m[A the violet-ness process takes complete charge.
The pigeon also seemed less sensitive to changes in wavelength than man,
though, unlike the fish, it pays much more careful attention to hues than
to brightnesses. Where man distinguishes 160 spectral segments, the
pigeon can discriminate only 20 between ?u700m|j, and A,460m[i; but of
course the bird's real capacity in this regard is concealed, in any training
technique, by its low intelligence. When a human observer is put under
instrumental handicaps similar to those of Hamilton and Coleman's
pigeons, he may be able to distinguish no more than 20 or 30 hues, as
Edridge-Green found. The pigeon was actually able to make discrimin-
ations where its human overlords could not; and probably, through the
instrumentality of the oil-droplet mosaic, it really has many more hue-
experiences than we can possibly help it to demonstrate to us (see p. 502) .

The activities of birds are guided almost entirely by vision, but they
are the stereotyped actions of an essentially stupid group of creatures.
The most intelligent of all birds are probably the parrots and their near
allies. The color vision of one of these, the budgerigar or Australian
zebra grass-parakeet (Melopsittacus undulatus) , was investigated by
Bailey and Riley in 1931, and independently by Plath in 1935. Bailey
and Riley were primarily interested in the budgerigar's ability to form
and break psychological associations with colors. Their study of its color
vision as such, while technically much more elaborate than Plath's, was
beclouded by misconceptions of the nature of hue and saturation. Plath's

500 ADAPTATIONS TO PHOTIC QUALITY

work, though based upon colored papers rather than filtered lights
(which the Canadians used) , yielded rather more useful information.

The budgerigar shows neither the blue-blindness nor the extra sensi-
tivity to red exhibited by the domestic fowl and other birds. Supposedly,
this is due to the fact that this bird lacks the deep red oil-droplets present
in both hen and pigeon. According to Plath, the parakeet has only
orange, yellow, and pallid greenish droplets. The species discriminates
blues and violets from grays about as readily as other colors. Grays are
distinguished from one another with difficulty (and are perhaps never
seen photopically, by any bird, untinged by oil-droplet colors). The
curve of hue-discrimination has two maxima, somewhere in the yellow-
green and in the short-wave regions — they could not be precisely located
with Plath's colored-paper technique. Violet was as often confused with
red as with blue, indicating a closed color circle.

Though many investigators have demonstrated a Purkinje phenom-
enon in diurnal birds by means of pupilloscopic, electroretinographic,
and training techniques, not much has been done by way of a compari-
son of the photopic vision of a single species with its own scotopic vision.
Rather, the photopic vision of diurnal birds has been contrasted with the
photopic vision of nocturnal birds, and a little has been done with the
scotopic vision of the latter.

Piper, in 1905, was the first to make such comparisons. He recorded
the retinal action currents under monochromatic lights, and found that
the eyes of diurnal birds, such as the hen and buzzard, all gave maximal
responses to A,600m[X, both when light- adapted and dark- adapted. Owls,
both scotopically and photopically, proved most sensitive to A,535m[l.
A Purkinje phenomenon for either type of bird was thus denied, though
one might speak here of an 'interspecific Purkinje phenomenon', bearing
out the Duplicity Theory just as well; for the diurnal birds have few
rods and the owls, few cones.

But no bird is known to have an absolutely pure-cone or pure-rod
retina, though some are suspected of having no rods and the most noc-
turnal of all birds {Apteryx? Steatornis?) may, when studied histologi-
cally, prove to have no cones. All duplex birds should show a Purkinje
phenomenon, and Piper's results have consequently been questioned
many times. In 1907, Abelsdorff first applied to birds the then recent
discovery of M. Sachs : that the responses of the pupil to lights indicate
directly the relative brightnesses of the lights to the animal. He found
the pigeon's pupil to be less responsive to green and blue than the human

COLOR VISION IN BIRDS 501

pupil. The pupils of four species of owls, on the other hand, contracted
more to blue than that of a man standing alongside of them. The pro-
cedure was to alternate the same two lights, respectively red and blue, on
the different pupils under the same adaptation conditions, watching to
see under which light the pupil closed the farther. Having available by
chance an intelligent, totally-color-blind man, Abelsdorff dimmed the
blue light until this subject's pupil remained unaltered during the alter-
nation of red and blue. Though these two lights were now equal in
brightness to the achromatic man, the pupil of an Athene noctua still
contracted farther under the blue than under the red. Similar behavior
on the part of the cat's pupil (in contrast to that of the dog, which
responds like man's) convinced Abelsdorff that the greater sensitivity to
blue in nocturnal birds and mammals is due to the greater concentration
of rods in their retinae — which also, of course, accounts for any dimin-
ished sensitivity to red light (such as occurs in rodents) , since the rods
are not stimulated by light which rhodopsin does not absorb. The lessen-
ed sensitivity of the pigeon to short-wave light was naturally explained
by Abelsdorff on the basis of oil-droplet absorption.

Laurens in 1923, and Erhard a year later, between them confirmed
Abelsdorff and accounted for Piper's peculiar findings. Laurens found
that the pigeon does indeed have a Purkinje phenomenon, but that it
takes all of 45 minutes for any discernible effects of dark-adaptation to
manifest themselves. Piper had not waited long enough to get actual
dark-adaptation, and consequently missed the Purkinje phenomenon; nor
had he, like Laurens, used light beams of equal energy content, and he
therefore obtained fallacious maxima. With equalized lights, Laurens
found that the pupil of the light-adapted pigeon responded between
A704m[i, and A,424m[X, maximally at A,564mp,. Scotopically, the spectrum
was shortened at the red end to A,664.5m^ and the maximum was shifted
to A524.5m[X. All wavelengths longer than 524.5m[l were lessened in
effectiveness by dark-adaptation, while the shorter wavelengths had in-
creased pupillomotor efficacy. Comparing the pigeon with man and the
alligator, Laurens found that in the pigeon the maximal contraction and
dilatation of the pupil were carried out much faster than in man (thanks
to the striated iris musculature?), while the alligator's contraction-time
was intermediate, its dilatation-time (because of cold-bloodedness, despite
striated muscles?) slower than that of either man or pigeon.

Erhard, also studying pupillary changes, found that short-wave lights
are brightest to owls, less bright to hawks, and least bright to fowls. This

502 ADAPTATIONS TO PHOTIC QUALITY

is in perfect keeping with the relative numbers of deeply colored oil-drop-
lets in the three types (see p. 197). Long-wave light had little stimulating
value for owls. Ten years later, however, Vanderplank made the surpris-
ing aimouncement that the tawny owl, Strix aluco, has a band of visi-
bility in the (human) infra-red, and thus sees its prey, in what for man
would be pitch darkness, by means of the prey animal's own body heat.
Vanderplank found that a strong beam of A,900m[i closed the owl's pupil
and seemed to dazzle and frighten the bird, though it had no effect on
the human eye. The owl could not find dead, cold prey or chunks of
meat in a darkroom — unless they were illuminated by an infra-red spot-
light.

Hecht and Pirenne have lately published contradictory findings,
though to be sure not on a close relative of Vanderplank's species of owl.
Working with Asio wilsonianus, the Americans found the curve of pupil-
lomotor effectiveness to be identical with the human scotopic brightness
curve (Fig. 35, p. 102), indicating that the photochemical system of the
owl's rod is the same as that of our own, and contains nothing in addition
to rhodopsin which could give it responsiveness to 'black' light. Vander-
plank might have been more perfectly refuted if Hecht and Pirenne had
chosen to work on Strix varia instead of Asio; but recently Matthews
and Matthews, studying S. aluco, have claimed that the eye makes no
response to black-body radiations from 40 C to 400 C, and that the
transmission of long infra-red wavelengths through the ocular media
is nil.

The spectral sensitivities of such birds, whose vision is certainly entirely
achromatic, are of little general interest. But considerable speculation has
been offered as to how the world of hues appears to diurnal birds. Natu-
rally, it depends upon the kind of bird — particularly, upon interspecific
differences in the oil-droplet mosaic. Where red droplets are numerous,
as in song-birds and fowls (and particularly in kingfishers), blues and
violets must be seen weakly and unsaturated. Hawks and woodpeckers
have few red droplets, parrots perhaps fewer still, or even none in some
species. The primary function of the droplets is not to produce hue-dis-
crimination (see p. 193) ; but they do necessarily influence the appear-
ance of colored objects profoundly. Tiny, uncontrollable eye movements
appose first one color of droplet, then another, then a colorless cone or a
rod, to a given point in the optical retinal image. Each point in space is
thus continuously 'scanned' by a succession of filters; and while at any
one instant these abolish as many contrasts as they enhance, in the next

COLOR VISION IN BIRDS 503

instant the pattern changes kaleidoscopically and the net result is en-
hancement of every contrast sooner or later — and all within a tiny frac-
tion of a second — making for a net improvement in visibilities in general.

The oil-droplets cannot, however, increase brightnesses. Though the
red and orange ones may be held accountable for £he partial blue-blind-
ness of so many birds, they cannot possibly be what makes the same birds
extra-sensitive to red light. Any such peculiarity is due to the photochem-
ical properties of the cones and to their high concentration in the retina.
We, too, would probably see reds more vividly in the retinal periphery,
if the latter were pure-cone like the fovea. The rods being blind to red
light, their interposition in large numbers between the cones is analogous
to sprinkling a piece of red paper with gray dots : at a little distance the
paper will appear homogeneous but unsaturated, its red chroma weak.
Rods lying between the cones of any duplex retina naturally unsaturate
all colors by intermingling a grayness-sensation with the colored one
from the cones; but in the case of red, they introduce darkness, for they
do not 'see' red even as grayness.

Hess was fond of saying that the bird sees the world as we would see
it through a pair of orange spectacles. Such a description perhaps covers
the dimming of short-wave stimuli, but scarcely the brightening, for the
bird, of long-wave ones. Moreover, though the blend of the bird's red
and yellow oil-droplets may theoretically be orange, the bird does not
have the effect of an orange droplet in each and every cone. If our bird's
eye view of things were taken through spectacles composed checker-
board fashion of minute red, yellow, and colorless areas, each just large
enough to subtend one cone back in the retina, analogous to the screen
of a Finlay or Dufay color-photo, we should then be able to gather some
idea of how things look to birds. Such a screen would have no such
action as that of a homogeneous orange filter.

The possibilities as to manipulation of the ratios of colors in the oil-
droplet mosaic are infinite ; and we may be sure that some of the extreme
ratios we can tally, as in hawks and parrots and kingfishers, and in the
red and yellow fields of the pigeon's retina, represent adaptations to
aspects of the various birds' ways of life, some of which are still quite
unsuspected. Some suggestions have already been given (pp. 195-8).
A promising viewpoint is that of Worth and Porsch, who, independently
of each other, have pointed out that red and 'fire' colors are extremely
common among the flowers which are visited by such birds as honey-birds,
humming-birds, etc., and which are dependent upon such birds for their

504 ADAPTATIONS TO PHOTIC QUALITY

pollination. Less common, but still very numerous among bird-flowers,
are blue-flowered species. Porsch relates the abundance of red-flowered
bird plants to the birds' high sensitivity to red (which has been experi-
mentally demonstrated for humming-birds), suggesting that the red of
the flower is an identification mark which the bird can pick out from a
great distance, and which remains maximally visible against the foliage
even in the auroral and crepuscular hours. He raises the question
whether flower-visiting birds may not have man-like or superhuman sensi-
tivity to blue light as well as to red — assuming that the plants have actu-
ally adapted their flower colors to fit the visual spectra of the birds upon
which they depend. Obviously, in the evaluation of avian oil-droplet
color mosaics and patterns of spectral responsivity, in ecological terms,
the surface has scarcely yet been scratched.

Mammals — Within the mammals, color vision is by no means wide-
spread, as it is in fishes, reptiles, and birds. To a large degree this is sim-
ply an expression of the fact that strong diurnality is uncommon in mam-
mals. But, not even all diurnal mammals have color vision. This would
be particularly hard to understand if the few diurnal mammals were all
primitive and stood closer than other mammals to the reptilian stem. The
birds, for instance, clearly owe their chromatic vision to direct, unbroken
inheritance from reptiles — possibly avian color vision traces back through
the reptiles to the Stegocephali, or even back through them to the fishes
(Fig. 156, p. 519).

The indications are, however, that on the road of mammalian evolu-
tion there was a considerable stretch of achromatic noctumality between
the color-seeing reptiles and the first color-seeing placental mammals.
Strong or strict diurnality, backed up by a cone-rich or pure-cone retina,
is not a primitive habit of mammals. Nor can it be said that diurnality
has arisen in the mammals only as one of the specializations and points-
of-superiority of the 'highest' forms. Though the larger ungulates and car-
nivores tend toward diurnality, in that they have become arhythmic from
nocturnal beginnings, it is only the squirrel and monkey tribes which pre-
sent fully diurnal members. The squirrels are rodents, which rank fairly
low — but even they must be given rank above us, in point of 'special-
ization' and 'modernity'. We, as primates, adjoin the very lowest of all
the orders of placental mammals, the Insectivora. All of our domestic
animals roost far higher in the taxonomic tree than we ourselves — a point
which is overlooked by some writers on comparative ophthalmology, who

COLOR VISION IN MAMMALS 505

would as soon as not derive some structure in the human eye from some-
thing or other in the eye of a horse.

Diurnahty, with its expectation of color vision, is thus a habit which,
so far as the mammals are concerned, has cropped out only in forms a
little removed from the bottom of the heap — and a great way from the
ungulates and carnivores which sit on top. In a survey of the mammals,
we can perceive no majestic progress in the evolution of color vision from
an imperfect system in primitive groups to a complex one in the highly
specialized orders. On the contrary, we find a fully-developed color
system only near the roots of the class, in the primates; and in the higher
subdivisions there are only the most rudimentary of color-senses, if any.
So, to avoid anticlimax, we can best review the subject of color vision in
mammals in reverse order, starting with the higher groups and progress-
ing to the lower ones.

The ungulates afford a classical supposition: that male cattle are in-
furiated by red objects. In 1923 Kittredge began some experiments with
a calf which yielded only negative results as far as they went, but were
unfortunately never concluded. In the same year Stratton summed up
some simple experiments as indicating that cattle pay as much attention
to green as to red, more yet to white, and are most aroused by any flut-
tering object, whatever its color may be — especially when the object is
unfamiliar. Red has no special emotional value, hence cannot be assumed
to arouse a distinct sensation quality. A whole herd of European stud
bulls were once provided with red veils, which entirely failed to disturb
their equanimity.

Oddly enough, the horse has never been the subject of any extended
study of color vision. Large animals are not in favor with psychologists
as experimental material, for obvious reasons; but even so, the docility
and intelligence of the horse qualify him admirably for exploitation. As
indications of color vision, however, we have only such items as the old
report that a French army horse, in North Africa, was able to distin-
guish his master in a red uniform from other men in blue ones, at a dis-
tance of 600 meters — a hundred meters farther away than he could make
the distinction without benefit of the color-difference in uniforms. But,
there is nothing here to show that the discrimination was on the basis of
hue rather than of brightness.

Among the carnivores, the dog, cat, raccoon, and two mustelids — the
European stone- or beech-marten and the polecat — have been studied.
Color vision was affirmed for the dog by Gates in 1895, Himstedt and

506 ADAPTATIONS TO PHOTIC QUALITY

Nagel in 1902 and 1907, and Colvin and Burford in 1909. Lubbock, in
1888, Nicolai and Orbelli in 1907 and 1908, denied it. None of these
investigators adequately excluded discrimination on a basis of brightness.
Nor was brightness controlled properly by Kalischer, working in this
period, though he did use colored lights. One of his dogs could distin-
guish a red light readily from a blue one, less readily from other colors.
One reaction which Kalischer did obtain, and which speaks strongly for
a qualitative perception of hue, was a sharp withdrawal of the dog from
a blue light.

The first impeccable experiments were those of Samoiloff and Pheo-
philaktova in 1907. They found that dogs confused colored papers with
gray ones of various shades; but they were not confused so consistently
as to make it certain that discrimination was wholly lacking. The best
results were obtained with green — the dog could not distinguish it readily
from dark grays, but showed some improvement with practice. When the
shape of the green paper was changed, the animal more often chose the
negative, gray paper which was of the old familiar shape. The investi-
gators concluded that form is far more important to the dog than color,
if indeed the animal experiences color at all.

Smith, in 1913, worked with seven dogs which she also trained to col-
ored papers. For any given color, some group of grays in her long Nendel
gray series gave the dog great difficulty in discrimination; but Smith was
unable to find any gray which a given dog would always confuse with a
particular color. The animals could tell grays from each other better than
from colors; but Smith concluded that at least certain individual dogs
have an unstable color sense, so very rudimentary as to be completely
unimportant to the animal. For the dog, it is form and (to a less extent)
brightness which are important qualities of visual stimuli. Whatever
weakly chromatic sensations his cones may afford are further unsaturated,
greatly diluted, with 'grayness' stemming from his superabundant rods.
To any such semi-nocturnal, rod-rich animal, the richest of spectral lights
could at best appear only as delicate pastel tints of uncertain identity.

For the domestic cat there is even less evidence of any color vision
whatever. Colvin and Burford, while they thought there was positive
evidence from their work in the case of the dog, claimed none for the cat.
De Voss and Ganson in 1915 reported a study of nine cats, in which
training to colored papers of controlled albedo and texture was involved.
For every cat and every color, a particular gray paper was found which
was completely confusing. When the training color was placed among

COLOR VISION IN MAMMALS 507

the 89 samples of the entire Bradley color set, the cat would pick out not
only it, but several others as well. Pavlov, it may be noted, was never able
to establish in the cat a conditioning of reflexes to hue, and was partially
successful with a dog only after 3000 trials.

Gregg et al, in 1929, attempted to train a cat positive and negative to
different combinations of filtered lights arranged like Ardois signals; but
when gray stimuli of equivalent brightnesses (for the human) were sub-
stituted for the various colors, the animal responded just as though the
colors were still there. The investigators concluded that the cat is totally
color-blind, or that at any rate colors have absolutely no significance
for her.

Only Kalischer has claimed that cats easily discriminate hues. His 1929
report on the subject is very sketchy. He claims to have varied the intens-
ities of his colored lights sufficiently to exclude a brightness-discrimi-
nation, but he does not give enough details to enable one to be at all
sure — especially when it is borne in mind that cats certainly see short-
wave lights much brighter (as indicated by their pupil responses) and
probably see long-wave ones much dimmer (because of the great predom-
inance of red-blind rods) than we do. It is particularly reprehensible, in
the case of nocturnal mammals, to assume that the relative brightnesses
of colors are the same as they are for humans. It can very reasonably be
assumed, always, that they are not. Another method of Kalischer's —
'training' the cat positive to undyed, negative to dyed, meat — is open to
the serious criticism that he made no attempt to rule out olfaction. So
finicky a feeder as the cat would assuredly need no training to avoid
food which did not smell quite right to her. We can be quite sure that
the cat has no hue-discriminatory capacity at all; and we might para-
phrase the old saw to read : "Day and night, all cats see gray."

None of the various researches on the raccoon is very complete. Cole's
first work, in 1907, was not properly controlled. With Long, in 1909, he
succeeded in getting raccoons to select a colored paper, or the gray, from
a series of five colors and one gray all of which had the same albedo (in
flicker photometry) for the human eye. These investigators also tested
the animal's ability to discriminate brightnesses, and found it excellent.
But their conclusion — that the animal has some color vision — was unjus-
tified inasmuch as they made no effort to match a color with a gray in
brightness for the raccoon. Davis, in 1907, was not even able to train
raccoons to colored stimuli which were of equal brightnesses for man.
Gregg et al, with the same procedure which had yielded only negative

508 ADAPTATIONS TO PHOTIC QUALITY

results on the dog and cat, obtained only negative results also with the
raccoon. This species is thus in the same boat with the dog : if it has any
color sensations, they are so vague and unsaturated that some individuals
are not even conscious of them at all; and to other individuals, they can-
not be made to have meaning.

Despite the alleged interest of the mink in red objects, the mustelids
which have been studied at all carefully have shown no evidence of hav-
ing color vision. Miiller, in 1930, dyed some hen's eggs red, green, blue,
gray, and white. His captive marten (Martes foina, a close relative of
our Martes americana) was allowed to come for them and take them,
one by one, to its cache in a corner of the cage. The animal took the eggs
in various sequences in successive tests, evincing no indication that any
one egg seemed brighter than another or that any color was especially
attractive or repellant. MuUer's extensive studies of the psycho-physiology
of this species led him to rank olfaction above hearing in importance for
the animal, with vision a poor third on the sensory list.

Miiller did more work with the polecat, Putorius putorius, a type of
mustelid for which there is no exact American counterpart, but which is
the wild ancestor of the domestic ferret seen here occasionally in the
capacity of professional rat-catcher. Miiller rated the sensory modalities
of the polecat all lower than those of the stone-marten, but in the same
order of value. The polecat could be trained to discriminate brightnesses,
but not colors. It was taught to distinguish between red and blue papers,
but when these were placed among other colored and gray papers the
animal was lost. The species is either totally color-blind or perhaps, like
the dog and raccoon, excessively color-weak. All in all, the evidence for
color vision in carnivores is practically nil.

Turning to the rodents, we find ourselves in a most controversial sub-
ject. On some of the selfsame species, equally strong claims both for and
against color vision have been advanced. While the squirrels are set off
sharply from other rodents by their diurnal habits and cone-rich or pure-
cone retinae, strangely enough the evidence for color vision in them is no
better and no worse than that relating to some of the most strongly noc-
turnal rodents, whose possession of any cones at all is questioned by
some retinologists.

In all, three kinds of squirrels, six other rodents, and one lagomorph
have had experimental attention. Most of the studies have been made
upon the common laboratory species. Watson and Watson, in 1913,
studied the rat with a spectral light technique. They trained rats positive

COLOR VISION IN MAMMALS 509

to yellow (A,595m^) and negative to darkness. When a blue (A,478m|i)
of low intensity was substituted as the negative stimulus, the rats con-
tinued to go to the yellow. But when the intensity of the blue light was
increased to a certain point, the rats broke down and made chance scores.
One rat was trained positive to red versus green. Removal of the green
stimulus confused the animal, which made chance choices; but removal
of the 'positive', red, stimulus had no effect. Obviously, the red stimulus
was no stimulus at all — the rat was blind to it. This shortening of the
red end of the spectrum is quite in keeping with the fact that the rat, like
all other known rodents, exhibits no Purkinje phenomenon either electro-
retinographically or pupilloscopically. This, despite the unquestionable
presence of some cones, in a proportion of perhaps one to every hundred
or more rods.

Munn, in 1932, used colored papers with the rat and obtained only
negative results. Several years later, with Collins, he reinvestigated the
rat's perception of red light. The red stimulus was paired with a 'nega-
tive' white light and with darkness in alternate sets of trials, the object
being to make impossible any step-wise response always to the brighter
stimulus, and to avoid giving the rat any constant stimulus to which he
could become negative. The animal was thus forced to react positively
to redness alone if it could; but it proved unable to do so with any regu-
larity. The authors concluded that for the rat the brightness-relation of
the stimuli was of most importance, their absolute brightnesses secondary,
and that color discrimination — if any — was indeed weak. These results
verified those of Muenzinger and Reynolds, whose technique had been
similar except for the use of red, white, and black papers instead of red
and white lights and darkness. The rat had shown an ability to discrim-
inate red from gray, but with great difficulty when the gray was close to
black. This again would be expected if the rat is blind to long-wave light.

The work of Coleman and Hamilton has been considered, by psy-
chologists, a model investigation. In 1933, they trained rats positive to
black versus red. When gray was substituted for the black, and when the
red was exchanged for a darker shade, the animals reversed their prefer-
ence. Reversal of the brightness relationship in other pairs of color
stimuli also inverted the responses of the rat. With some pairs, only
chance scores were ever made, showing that the two stimuli were not only
matched in brightness but had no difference for the animal as to hue.
WTien new rats were introduced to these 'confusion pairs' of colored
papers, they could never learn to go to one paper and avoid the other.

510 ADAPTATIONS TO PHOTIC QUALITY

Walton, however, has insisted that the rat has color vision. In 1933,
he trained rats to large patches of filtered colors, the two members of
each pair of stimuli being matched in brightness for the human eye at
first. The animals readily learned to discriminate red from green, blue,
and yellow, and to tell blue from yellow. Their discriminations of green
from blue, and of yellow from green, were not high but were better than
chance. When one member of a pair was increased in brightness, the
animals continued to make the proper choice. Walton concluded that
the rat has hue sensations; but the Watsons had shown that the rat's
brightness curve is enormously different from man's, and Walton made
insufficient efforts to find a point of matched brightness for any pair of
stimuli. With Bomemeier in 1938, Walton used red and blue stimuli and
satisfied himself that the rat discriminated them solely on a basis of hue.
His animals also discriminated red versus darkness; but, far from the
red's being all but invisible to them, they behaved as if they were 'rather
sensitive' to it when in a condition of semi-dark-adaptation.

Walton's methods are not sufficiently different from those of other
students to make it at all easy to see why he gets such unique results.
Majority opinion seems to be that until his work has been abundantly
confirmed, it must be held to conceal some unknown errors of procedure.

For the house mouse, as for the laboratory rat, the great weight of
evidence is negative; yet here again a single investigator has claimed
positive results with what seems to be adequate technique. In his classical
study of the dancing mouse in 1907, Yerkes reported that the mouse
could discriminate between filtered green and blue lights only when they
differed greatly in intensity. Green versus red, and blue versus red dis-
criminations were easily learned; but when any colored light was replaced
by colorless, the mouse went to the less bright of the two stimuli. Red
light was only responded to as the brighter of two lights when it was of
very high intensity. As in the case of the rat, the spectrum of the mouse
appears to be shortened at the long-wave end.

The preference for dim lights is in interesting contrast to the mouse's
strong preference for white and bright-colored papers (as nest-building
material), as reported in 1934 by Kolosvary. This worker's animals pre-
ferred blue paper to red however, which would be expected from his
other results since the invisibility of the redness of red papers would
naturally make such papers appear dark to the mouse.

Hopkins, rejecting the work of Yerkes and the later, also negative,
findings of Waugh and Roth, described in 1927 some experiments on

COLOR VISION IN MAMMALS 511

mice with both normal and 'hereditary rodiess' (Keeler) retinae. He
found reason to think that some individual mice have a rudimentary
color sense. Most of his animals could not discriminate colored papers
from grays or colored lights from white ones, but one mouse out of seven
could distinguish a red light from a white one — though the same individ-
ual confused red papers with gray ones. But we should expect that if red
light is of no stimulating value it would naturally be discriminated (as
darkness) from even a dim white light, whereas a red paper would not
be invisible, even though its redness was not registered, but would appear
gray and would be confused with gray papers. Despite this sort of criti-
cism of his work, Hopkins remains to the mouse what Walton is to the
rat: the sole claimant of color vision; and the same remarks apply to
both — their techniques are not discernibly superior, if equal to, those of
the larger number of other investigators who have found no reason to
think that murid rodents see hues as such.

The rabbit has come in for some attention. The Watsons found, as in
the case of the rat, that after red-versus-green training, darkness could be
substituted for the red light without disturbing the animal in the slight-
est: red light is darkness for the rabbit. The animal was now trained
positive to a blue light and then was required to discriminate it from a
dim yellow, which was gradually brightened. The animal died before the
investigators were able to try a range of intensities sufficiently great
to exclude a brightness discrimination. They were only able to say that
blue light probably looks brighter to the rabbit than a yellow of the same
energy.

At about the same time (1912) Washburn and Abbot were experi-
menting with six rabbits, using colored papers. The animals learned to
distinguish a red from a light gray, but could not tell the red from a dark
gray or a black. The results with blue-gray discriminations were not so
striking, but did permit a conclusion that only brightness guided the
rabbit to a choice.

Again, as with the rat and mouse, there is conflicting evidence. R. H.
Brown, in 1936, claimed to have established a Purkinje shift in the
rabbit, from A,560m[i, to A,530m[l; but his procedure was altogether too
crude to support his conclusions. He established a reflex response to
colored light by conditioning with light and shock stimuli. His animals
were quickly made responsive to only one member of a pair of lights
(A,640m[l and ^490m[x), but his variation of the intensity of the nega-
tive stimulus was made in only three large steps — scarcely adequate to

512 ADAPTATIONS TO PHOTIC QUALITY

spot a point of matched brightnesses. Brown's technique is promising, but
in his hands it has yielded no evidence of color vision in the rabbit.

Another piece of work which would bear careful repetition is that of
Sgonina, in 1936, on the guinea-pig. This animal's retina is even more
certainly a pure-rod one than that of the rabbit; yet Sgonina claims that
it is able to discriminate between colored papers whose difference in
brightness is less than that which must exist between two gray papers, if
the guinea-pig is to discriminate the latter. He found that two grays
could be told apart only when one was about one-third brighter than the
other. The validity of his conclusion obviously hinges upon the correct-
ness of the assumption that a guinea-pig sees the brightnesses of colored
papers as Sgonina himself did — and we have seen, ad nauseam, that such
an assumption must never be made.

Salzle, also in 1936, studied two species of wild mice. He found that
despite its excellent learning capacity, the European long-tailed field
mouse (Apodemus sylvaticus) was hopelessly confused when a red light
was offered it alongside a yellow or green to which the animal had been
trained to go. The red-backed mouse (Clethrionomys glareolus) told a
different — and unique — story :

Animals trained to filtered red light readily learned to distinguish it
from green, blue, and yellow. Animals trained to green quickly learned
to discriminate it from red; but when offered green versus yellow their
discrimination was poor and, though it improved rapidly, never became
perfect. Offered green versus blue, they failed completely. Salzle then
trained two animals to each of the four colors, and offered each of the
animals all four colors at once, their positions being changed from trial
to trial to avoid position habits. The result was that the animals trained
to red or to yellow went mostly to red or to yellow as the case was, but
the animals trained to green went about equally to green and blue, and
the animals trained to blue went equal numbers of times to blue and to
green. Salzle was sure that the apparent equivalence of the green and
blue stimuli was not due to their being matched in brightness for the
animal — but his evidence for this was that the green light was much
brighter than the blue one for his own eye. We would expect a human
green-blue brightness-match to be no match to achromatic rodents; for
their scotopic and photopic brightness curves appear to rise from zero in
the red to a maximum in the blue-green or blue. A green which matched
a blue for them would look brighter than the blue to a human.

COLOR VISION IN MAMMALS 513

The two green-trained animals were now investigated further, with one
green and three blue stimuli offered simultaneously in varied positions.
Assuming that the animal could not discriminate the stimuli, it should
have gone 25% of the time to the green stimulus and 75% to the various
identical blue ones. One of the mice went to green ten times and to blues
38 times (21%-79%). The other went to green 16 times and to blue 32
(33.3%-66.6%). Salzle felt confirmed in his judgment that for this
animal green and blue are qualitatively identical. He attempted, quite
unsuccessfully, to fit this into the framework of either the Hering or the
Young-Helmholtz theory of color vision. But the strong probability is
that the animal is achromatic and that the particular green and blue were
a match for it in brightness — Salzle is most vague concerning his alter-
ations of intensity, and his text gives no assurance that this factor was
controlled.

Lastly, for nocturnal rodents, may be mentioned Sackett's (1913)
negative results with the porcupine. The absence of color vision in
such rodents, all of which have few cones (or even none), is no sur-
prise. But in the diurnal squirrels, whose retinae contain no visible amount
of rhodopsin and appear to contain only cones (this being certain in the
case of the ground-squirrel and prairie-dog), color vision would be ex-
pected— indeed, a color vision about as rich as that of our own foveal
region, though of course affected in the short-wave realm by the presence
of a yellow filter, the lens (see p. 199). In the light of this expectation,
the results of experiments on squirrels are most interesting :

Colvin and Burford, in 1909, were able to train a native squirrel posi-
tive to a pigmentary red and negative to either another color or a gray,
all the stimuli having the same brightness to man. They drew the un-
warranted conclusion that the squirrel, like their dogs, discriminated the
hues as such. Salzle also worked on one specimen of the European
squirrel iSciurus vulgaris) , training it first positive to green, then to red,
and offering three negative color-stimuli with each. The animal had no
trouble in making all discriminations. Salzle states that with each pair of
lights, one or the other could be made brighter or darker, or the two
about the same brightness (for his own eye) without it making any differ-
ence to the animal's ability to tell them apart. But no attempt was made
to match their brightnesses for the animal, and no details are given as to
just how intensity was varied.

In contrast to these imperfect and inconclusive studies we have the
extremely careful work of Charlotte Locher which, though offered as a

514 ADAPTATIONS TO PHOTIC QUALITY

preliminary report, seems a truly model investigation. She reported, in
1933, on three Sciurus vulgaris, which she had trained with red, blue,
yellow, and green papers and with the Hering series of 30 grays. The
first animal was trained positive to red versus gray, and proved unable to
discriminate red from any dark gray. Substitution of another gray for the
red produced no disturbance in the sensitive creature, indicating that the
squirrel sees red objects as gray. It would go to the darker of two grays,
and when offered a blue versus a (darker) gray the animal did not go to
the blue at all until after three days of trials.

The second animal also failed to discriminate red from dark grays,
and could not distinguish green from light grays. Yellow was discrim-
inated from the very lightest grays about three times out of every five
trials, and was readily distinguished from medium and dark grays. Green
was completely confused with the three lightest of the grays. This indi-
vidual, then, saw red and blue as dark gray, green as a light gray, and
yellow probably as a very light gray, though the possibility of a quali-
tative difference of yellow from gray could not be denied.

The third squirrel had no trouble whatever in telling yellow from all
grays and white. Unless the yellow paper appeared to him even brighter
than white (which is possible, but seems unlikely in view of the perform-
ance toward green and blue) this means that the animal saw yellow as a
distinct quality. It was also able, after extra practice, to discriminate light
green from all grays, though it never learned, in 236 trials, to tell a rich
green from the darkest gray. It was also very difficult for this individual
to learn to tell blue from grays, though it finally succeeded in maintain-
ing an 80%-correct average on the most troublesome sequence of five
adjacent grays. Red was confused completely with all but a few of the
lightest grays, as in the other two squirrels.

Of Sciurus vulgaris, one can apparently say about the same thing as of
the dog : a weak hue-discriminatory capacity may be present — ^but so very
weak that, within the limits of normal individual variation, it may be
entirely lacking in a particular individual.

The ground-squirrels are even more certainly pure-cone than the tree
squirrels typified by Sciurus spp. One of them, the souslik (Citellus
citellus, the European counterpart of our thirteen-lined spermophile) was
studied by Kolosvary; but only as to color preference. When offered
strips of white and red paper as nesting material, the animal at first took
twice as many white ones as red, later became used to the red and took
about equal numbers of both. When white, blue, and black strips were

COLOR VISION IN MAMMALS 515

given, the souslik preferred the blue strongly, and white and black
equally. Given red, white, and blue pieces, it took blue slightly oftener
than white, and either about twice as often as red. This order of prefer-
ence— blue first, then white and black equally, then red — does not quite
check with the tree-squirrel's preference always for the darker of two
stimuli. The lens of Citellus is so strongly yellow that blue paper should
appear darkened, as red does to Sciurus rulgaris or to nocturnal rodents.
Even the vulgaris lens, which is probably pallid compared with those of
other squirrels, absorbs some light from A,436m|l on — all light from
A,400m|i, onward, according to Merker. But the equal value of white and
black for the souslik seems a paradox.

Leaving the rodents, we come at last to the primate order. Here, as
with the birds, there has never been any doubt of the occurrence of color
vision in all its glory. Among the species in the higher (Anthropoidea)
sub-division of the order, the chimpanzee, the Guinea baboon iPapio
papio), the pig-tailed macaque (Nemestrinus nemestrinus), Pithecus
jascicularis, the rhesus monkey, the sooty mangabey {Cercocebus tor-
quatus) , squirrel and spider monkeys have all been studied. The work of
Kinnaman (1902), K6hler (1918), Bierens de Haan (1925), Kohts
(1928), Trendelenburg and Schmidt (1930), KlUver (1933), Brecher
(1936), and Grether (1939, 1940, 1941) on these forms has shown that
their hue systems are identical with the human one to all intents and
purposes. None of this work whatever is negative in implication.

The few investigations to date upon the lower primates, the Lem-
uroidea or Prosimiae as opposed to the Anthropoidea or Simiae, have
yielded only negative results. In general, this is to be expected, for most
of these lower forms are strongly nocturnal whereas all of the higher
primates except the douroucoulis or night monkeys (genus Aotus =Nycti-
pithecus) are diurnal. Some, at least, of the prosimians are pure-rod.

But among these lower primates there are two groups of genera whose
habits are opposite to those of all other lemuroids — just as Aotus stands
out as a rebel among the anthropoids. These are in the sub-families
Indrisins and Lemurinse. In the former, the avahis (genus Lichanotus)
are strictly nocturnal, but Propithecus is diurnal and crepuscular and
the black indris ilndri indri) is diurnal. Among the lemurines there are
also several nocturnal genera; but Hapalemur is diurnal and so are all
of the many species of Lemur itself.

One of the true lemurs, Lemur mongoz, was investigated in 1930 by
Bierens de Haan and Prima, who fully expected the species to exhibit a

516 ADAPTATIONS TO PHOTIC QUALITY

full color-vision system like that of other diurnal primates. One of their
two specimens proved to be totally color-blind. Trained to colored
papers, it was confused by gray ones — by dark grays with red and green,
medium grays with blue, and by light grays apposed to yellow stimuli.
Only a training-to-brightness was possible; and this was readily switched
over from responses to red versus blue to green versus yellow stimuli, and
from green versus yellow to dark gray versus green. In both of these cases,
a color-seeing animal would have been quite befuddled by the change.

The second individual was trained to blue only. It could then be con-
fused by grays of a particular sequence, but did somewhat better as time
went on. This lemur was disturbed when switched from blue versus red
to light gray versus red; but since for the other animal blue was matched
by medium grays, differences in behavior toward blue and light gray are
not at all surprising and prove nothing as to color vision.

The authors consider that if an animal makes no more than 30% errors
in a color-versus-gray discrimination it cannot be considered totally color-
blind. But, even if such a liberal allowance be made in this instance, we
cannot credit the lemur with having any more vivid color experiences
than the carnivores and the rodents. The situation in the lemurs — in
which diurnality is already firmly entrenched but whose color-sense is
only in its faintest beginnings — is the best of evidence for thinking that
primate color vision has arisen wholly within the primate stock.

The situation in Cebus, as reported by Grether (1939, and in cor-
respondence with the writer) is especially interesting. Grether's four
individuals, of two species (C. unicolor and C. capucinus) , all gave every
evidence of being protanopic dichromates, with lowered sensitivity to
red and with a neutral point at about A,515m[X. Watson's (1909) data
on one Cebus are reconcilable with Grether's findings, though Watson's
procedure was not such as to reveal dichromasy in his animal. This one
genus, then, may have a dichromatic system as its standard equipment.

The diversified Cebidae and the more homogeneous Hapalidae (mar-
mosets) comprise the platyrrhine (New- World) division of the Anthro-
poidea, opposed to the catarrhine series of Old- World forms. The
platyrrhines and the catarrhines are usually considered to have had quite
independent origins from lemuroid stock. If the lemuroid ancestors of
both had color vision, then all primate color vision stems from a single
beginning. If however the lemuroid common ancestor of all the monkeys
lacked color vision — as seems likely — then color-vision systems have
developed separately in the platyrrhines and the catarrhines. Again,

COLOR VISION IN MAMMALS 517

while all catarrhines are diurnal and trichromatic, there remains a pos-
sibility that the trichromasy known for some cebids (e.g., the squirrel
monkey, Saimiri sciurea, and the spider monkey, Ateleus ater) has
evolved through a dichromatic phase in other cebids {i.e., Cebus).

The marmosets are less distinct from lemuroids than are the lowest
catarrhines, and may be ancestral to the Cebidae rather than derivatives
thereof — no one can be sure. In any case, nothing is as yet known about
their color vision. Among the cebids the nocturnal, assuredly achromatic
Actus may be the most primitive,* though this honor is usually accorded
to the closely-related diurnal genus Callicebus, whose color-vision status
is unknown. A case, of sorts, could thus be made out for considering
that trichromasy has evolved independently in the catarrhines and platyr-
rhines, and through achromatic (Aotus? marmosets?) and dichromatic
(Cebus — and Callicebus?) stages in at least the platyrrhine series, if not
through equivalent (but missing) links on the catarrhine side.

Below the primates there lies but one order of placental mammals, the
Insectivora, regarded by taxonomists as ancestral to all other placentalia
and as immediately ancestral (even osculant, through such forms as
Tarsius) to the primates. Some insectivores (the tree-shrews, Tupaia)
are strongly diurnal; but their vision has yet to be investigated. Only the
common European hedgehog, Erinaceus europceus, which is nocturnal,
has had attention.

Herter and Sgonina reported on this animal in 1933 and 1934. They
could not get their hedgehog to go to a yellow paper and avoid a blue
one — it insisted on going to the blue, so the investigators allowed that to
be the positive stimulus. Subsequent substitutions of other colored and
gray papers for the original stimuli revealed that the animal would
usually choose the darker of any two stimuli. The results suggested that
the hedgehog could see yellow, but no other color, as a quality distinct
from gray; but this conclusion hinged upon the outmoded Hessian
assumption that equal brightnesses for man are equal brightnesses for
animals. This is extremely unlikely in the case of the hedgehog, a noc-
turnal, apparently pure-rod animal. Miss Locher has offered other criti-
cisms, which Herter and Sgonina have failed to eliminate in their second
contribution. The hedgehog may have a color-life comparable with that
of Locher's second squirrel, but it probably has no color vision at all.

*Though the fact that its tapetum is utterly different from that of the lemuroids (p. 233)
suggests rather that the noctumality of Aotus is secondary.

518 ADAPTATIONS TO PHOTIC QUALITY

Of possible color vision in some of the most nearly diurnal marsupials,
the kangaroos and wallabies, we know nothing. For the monotremes and
marsupials together, there is only the single entirely negative report of
Salzle on an opossum species, Didelphis paraguayensis. But the retenti<!^n
of the cone oil-droplets during so much of mammalian evolution, past
the monotreme level and into the marsupials, suggests that these lower
subclasses were not always as strongly nocturnal as their surviving repre-
sentatives (the kangaroos excepted) are today.

Phytogeny of Color Vision — In digesting the above survey, the
reader may have been struck by the fact that the groups of vertebrates
which possess full-blown color vision are the very ones which have
evolved excellent mechanisms of accommodation: the teleosts, the sau-
ropsidans, and the primates. This relationship is not accidental. These
are the groups which are more eye-minded than otherwise, and whose
retinal visual acuity is high enough to deserve refined optical images and
to make hue-differences a useful factor in the perception, identification,
and evaluation of visual objects. They are the only groups in which a
fovea is ever seen. The bright-light habit depends upon cone-richness,
affords high visual acuity, demands good accommodation, and supports
good hue-discrimination. It is only natural, then, that these phenomena
are found in association.

The color-vision systems of these three vertebrate groups are probably
just as independent of each other, in point of origin, as are their methods
of accommodation. If they are physiologically identical or nearly so (and
they certainly appear to be), it is because, like so many other simpler,
discontinuously-distributed and repeatedly-evolved entities (lentiflavin,
rhodopsin, melanin etc.) they have developed out of a substrate of chem-
ical and physiological potentialities which is common to all vertebrates.
In other words, the systems are homoiologous.

We know nothing about the possible color vision of non-teleost fishes.
The lampreys, some species of which have at least 50% cones, may con-
ceivably have it, though it would be hard to say what its value might be
to them. The elasmobranchs are all pure-rod excepting Myliobatis aquila
and Mustelus spp., which have few cones. But at least one of the hol-
osteans, Amia, is known to have a teleost-like retina and habits; and
when eventually investigated this may prove to be the group which really
invented teleostean color vision.

The extinct crossroads group of the Stegocephali, which were almost
certainly diurnal, may have shared with the teleosts the inheritance of

PHYLOGENY OF COLOR VISION

an original chondrostean color-vision system, and may have passed it
on to the reptiles and, through them, to the birds on the one hand and
the mammals on the other (Fig. 156). If so, the modern amphibians
lack color vision because they have discarded it as something useless in
their mode of life. Since no living color-seeing forms bridge the gap

[Higher Placentals|
|Pnmates)lMC:z::;^ ' I

[insectivoresi

COLOFf VISION:

PresenI |

Probably present —
Possibly present — [^

— D

Absent -

Fig. 156 — The probable phylogeny of color vision in vertebrates.

between the turtles and the fishes, we probably have no right to suppose
that the sauropsidan and teleostean color-vision mechanisms represent
only one single invention of long duration and wide distribution — at
least, not until the holosteans are shown to discriminate hues. Unfortu-
nately, no diurnal chondrosteans are left on earth.

520 ADAPTATIONS TO PHOTIC QUALITY

Exclusive of the placental mammals, then, color vision has been
elaborated perhaps only once (by the chondrosteans, passed on by
them to the stegocephalian-reptilian-avian series as well as to the teleosts) ,
perhaps twice (by the holosteans or teleosts and later, independently, by
the early reptiles [cotylosaurs], which gave it to the birds and maybe to
early diurnal mammals). Then too, color vision may have been devel-
oped de novo within some reptilian groups. For, just as the transmutation
of cones into rods in such forms as Sphenodon, the geckoes, and the
Xantusiidae may not necessarily have abolished color vision (gecko rods,
Crozier and Wolf have found, respond to flicker like turtle cones) , so
also color vision may have been regenerated or re-invented where cones
have secondarily reappeared. Dryophis et al will be most interesting in
this connection — if color-vision researchers sometime find a way to
'motivate' them — as would also the diurnal geckoes such as Phelsuma,
whose visual cells were once lizard cones, then gecko rods, and are now
probably cones once more.

However few or many times color-vision mechanisms may previously
have arisen in vertebrate evolution, the color vision of the higher pri-
mates is assuredly a law unto itself, genetically and historically speaking
(see Fig. 156). The absence of color vision in the lowest primates, the
lorises, galagos, tarsiers and the like, might mean only that these had dis-
carded color vision by discarding cones in order to become nocturnal.
The indications are overwhelmingly against such a view. The primates
originated as a nocturnal group, from nocturnal, rat-sized insectivore
ancestors which may not even have kept any of the cones of their
therapsidan forebears.

The placental-mammalian cone looks most suspiciously as though it
had arisen by transmutation within the subclass. It is never double, never
has an oil-droplet or a paraboloid, never migrates. The placental mam-
mals evolved through the restrictions of the nocturnality of the early
insectivores. Like the snakes, which had an even worse time being born
from the lizards, they probably produced an entirely new crop of cones,
which consequently are quite unlike those of the lower mammals and the
Sauropsida. Holding this viewpoint, it becomes easier to understand why
it is that although cones are numerous and widespread among arhythmic
and diurnal placental mammals, yet color vision is not. To acquire color
vision, each group of such mammals would have to start from scratch;
and only those have made this start, whose vision means so much to them
that color vision is a real desideratum.

PHYLOGENY, LOCUS OF COLOR VISION 521

Just as diurnality has surely arisen by slow degrees within the primate
group, so also has human color vision developed entirely within the pri-
mate order. We might expect to see color vision in the true lemurs — as
also in the diurnal squirrels — but it is not there. Only entirely above the
lemuroids has the final refinement of color vision been added to the pre-
requisite diurnaUty, and it is quite possible that this addition has been
made independently in the platyrrhines and the catarrhines (v. s.) .

It seems necessary to believe that human color vision owes nothing
whatever to the product of the teleost and the reptile. But 'human' color
vision is already present far below man in the anthropoid stock. It is not
necessary to suppose, with Bierens de Haan and Prima, that human color
vision has evolved wholly within the genus Homo. True, it was once be-
lieved that the ancients of Greece and Egypt had an incomplete color
vision as compared with modem man. The situation is now realized, how-
ever, to have been due to a simple paucity of words for colors in the lan-
guages of archaic and primitive peoples — the Homeric vocabulary, for
instance, contained no word for 'blue'. The Japanese use the word ao for
both green and blue — but they see a difference between them.

Locus of Color Vision — We know that whenever color vision did
arise, however often it may have done so, it involved a differentiation of
several cooperative sensation-processes in the central nervous system, as
well as a set of differentially photosensitive chemical substances in the
visual cell (see Chapter 4). These latter, however, may be universally
present in cones, several such substances being needed in order to fill out
neatly the responsivity of the visual cell, to embrace as fully as possible
the spectrum which the watery dioptric media of the eye will let through.
It seems highly significant that the electrophysiological images of hue-
stimuli show the same hue-specific character in achromatic animals (e.g.,
cats, rabbits) that they show in color-seeing forms. The evolution of a
color-vision system very likely entails only the affiliation of specific cen-
tral processes of registration and integration with particular photo-
chemicals already present in the cones.

Where, in the central nervous system, are these hue-sensory processes
placed? We can say a little, though not much, on that point. In the
lower vertebrates, the optic nerves (in their continuation as the optic
tracts, quite unmodified since the decussation is total) sweep directly up
to the optic tectum, the roof of the mid-brain. A few fibers do terminate
in other minor centers; but the connections of the tectum with the centers

522 ADAPTATIONS TO PHOTIC QUALITY

controlling extra-ocular, intra-ocular, and skeletal muscles make the optic
tectum very much the chief center for visual reflexes. Whatever visual
consciousness a fish may have — including the awareness of hues — must
reside in the optic tectum. There is no 'higher' visual center in the fish
brain. But there are connections of the tectum with other brain regions,
some of which might be vital to visual associations, Nolte, however,
working with Phoxinus and Gasterosteus, found that the removal of
such of these regions as could be destroyed without killing the fish,
failed to disturb the learning of associations with color stimuli. He
extirpated in turn the cerebral lobes, the habenular ganglia, and the
molecular layer of the cerebellum. The fishes still responded to color;
and others, which were trained to colors only after such operations,
learned in the normal time.

We might expect that even in the highest vertebrates much of visual
consciousness, including perhaps hue-consciousness, would continue to
be mediated by the homologues of the optic tectum, which are the
superior collicuH. But in the evolution of the nervous system the superior
colliculi have become very decidedly a spur track of the visual pathway,
and are concerned only with relaying impulses for reflex and willed
movement to the extra-ocular and other muscles (see Fig. 123, p. 335).
We have seen (p. 336) that in man all visual sensations reside in the
cortex, where color sensations are most susceptible of all to injuries of
the visual area in the occipital lobe. In man, the lateral geniculate nu-
cleus may play a considerable role in vision; but the optic tectum is
purely a reflex center and has surrendered, to the geniculate and the
cortex, any functions in visual sensation which it may have had in the
fishes and amphibians. Although the teleostean and primate color-vision
systems may be physiologically identical in their dependence upon three
elementary central processes, it would seem that they must be very differ-
ently localized in the respective central nervous systems — in the optic
tectum in the one, and in the lateral geniculate or in the cerebral cortex
in the other. The location of color vision in the brains of reptiles and
birds is a problem which has had no attention, though it should be
susceptible of experimental attack.

In the detailed localization of the color-sense within the primate cor-
tex, an interesting start was made a decade ago by the Swedish neurol-
ogist Henschen. He found that in layer IV of the visual cortex (see pp.
334-7 and Fig. 123) two different types of ganglion cells could be seen
in species having duplex retinas. Henschen identified these two types as

LOCUS OF COLOR VISION 523

'light-cells' and 'color-cells', and believed them to have ultimate connec-
tions respectively with the rods and cones of the retina. Color cells were
especially numerous in Nemestrinus, which has a fovea and has been
shown to have color vision. They were sparse in Lemur macaco, which,
though diurnal and provided with an area centralis (if not a fovea),
probably has no more color vision than L. mongoz (v.s.). Color cells
were entirely lacking in the pure-rod Perodict'tcus potto, which Henschen
consequently suggested would prove to be the only primate, among those
examined by him, entirely devoid of a color sense.

These investigations have never been carried further; but it would
be most interesting to compare, for example, the layer IV's of diurnal
squirrels and flying-squirrels — one might find that the two types of
cortical cells represented rods and cones right enough, but not neces-
sarily achromatic versus chromatic sensory capacity. More interesting
still would be someone's demonstration of an analogous histological
duplicity in the visual centers of some of the many sub-mammalian
possessors of duplex retinae, known either to have color vision, or not
to have it.

(B) Dermal Color-Changes

No class of vertebrates is lacking in members which, from time to time,
alter their color patterns by some means or other. There are vast differ-
ences from group to group as to the means employed, the length of time
involved, the facility and frequency of the changes, and their biological
values. The basic color patterns themselves, and those of animals which
cannot change them at all, may or may not be demonstrably adaptive in
particular cases. The somber colorations of strictly nocturnal mammals
are almost certainly not, for they pass unseen anyway. But we like to
think that the vertical stripes of a tiger help to hide him in a canebrake.
Fishes are dark above and pale beneath, so that they blend with the bot-
tom or with the bright water surface depending upon the point of view
of the beholder. We feel sure that this pattern is adaptive — and feel con-
vinced when we are confronted by such a phenomenon as the African
catfish Synodontis, which swims upside down and whose reversed color-
ation is expressed by its Arabic name, 'batensoda' i.- 'black belly') .

To be sure, the theory of warning and protective coloration is in dis-
repute as regards any universal applicability; but there remains an un-
shakable residuum of evidence that concealing colorations exist and actu-
ally do protect. There have even been experimental demonstrations. In

524 ADAPTATIONS TO PHOTIC QUALITY

Italy, there are both green and brown varieties of the praying mantis.
In 1904, di Cesnola tethered 20 green mantids in green grass and 20
brown ones on some brown, withered grass. Seventeen days later, all
were still alive. When he tethered 25 green mantids on brown grass, all
had been eaten, by birds etc., eleven days later. Of 45 brown insects
placed in green grass, 35 were dead in seventeen days. Similar experi-
ments, with similar results, were made years ago by Poulton, Sanders,
Crampton, Bumpus, Davenport and Weldon, and more recently by
Carrick, Young, Gerould, and Isely.

Very recently, the protective value of changeable coloration has been
shown experimentally by Sumner. When his fishes (Gambttsia) were
allowed to adapt to the shade of their background they were far less
often caught by penguins, herons, and predaceous fishes than other in-
dividuals placed in tanks which they did not match. Certainly, adaptive-
ness of an animal's coloration is the more likely, the more that coloration
is altered by the animal. If the alteration is adaptive, we must suppose
that the pre-change pattern had been adaptive, and has ceased to be so
under the conditions which produce the change. Sometimes — as in most
lizards — the change has nothing whatever to do with making the animal
less conspicuous. In such cases, we have a right to look for other ways in
which the change may yet be interpreted as adaptive to some end or other.

Modes of Color Change — The warm-blooded animals are under strict
limitations as to the changes they can possibly make. Their colorations
reside in lifeless hairs and feathers. They can sometimes be altered
quickly — locally — by skin muscles, as when a pronghorn displays his
white rump-patches, or when a running antelope-jackrabbit turns white
in its flight by revolving the belly skin up onto the side toward the pur-
suer and laying back his ears. But when a weasel or a willow ptarmigan
prepares for winter by turning white practically all over, it is by the ardu-
ous growth of new, white hairs or feathers and the shedding of the old.
One can cram a canary with foods rich in carotene, but the resulting
golden-yellow color will appear in the plumage only after the next sea-
sonal moult. Similar passive changes can be forced even upon man by
manipulation of his diet, or by exposing him to the sun until, in self-
defense against ultraviolet light, he becomes tanned by increased melan-
ization.

The fishes, most amphibians, and many reptiles expose to view living
pigmented tissues over the whole surface of the body. For some of these
animals, color changes may be only seasonal, as in the adoption of a

KINDS OF COLOR CHANGE

525

special nuptial pattern for the breeding period. The changes may be
local, as in the spreading of a lizard's throat-fan by engorgement with
blood, which then shows red through the transparent skin, or in the blush
of an excited macaw, which has a similar basis. But in large numbers of
species, relatively rapid changes are made by the whole skin in sympathy
with the time of day, temperature, humidity, or the shade or color of the
background. Even the nuptial coloration can be put on or off at a mo-
ment's notice by some jfishes, such as the cichlids and the red-bellied dace
iChrosomus) . These rapid changes were first produced experimentally
by Stark in 1830. They are possible because the dermal pigment, or a
good part of it, is contained not in inert cells or in defunct or cornified
tissues, but in active star-shaped cells. These were discovered and named

....•' .

''*'-.,

^(VBIM

• .

1 •

%.^^*^HB

• ' •

■ ■ ^ -

• .*■•

^"^1

♦ ^

r V

•4.

*^

. T ♦ V*

^*^N

«

"i'i _

#5 -

Wte;r:--

• *^

*

• [^

Fig. 157 — Dermal chromatophores of Fundulus heteroclitus; identical chromatophores are
similarly numbered in the two piaures. From Parker, after Spaeth.

a, contracted; h, expanded condition of pigment masses.

'chromatophores' by Sangiovanni in 1819; and in 1860 Kolliker, study-
ing a lung-fish, Lepidosiren, first showed clearly how they work to
change the appearance of the animal.

Only while they are developing do these chromatophores ever actually
change their shape. In fully-formed chromatophores, the cloud of pig-
ment granules within the cell may be swept into a compact mass by cen-
tripetal cytoplasmic streaming, or dispersed uniformly out into the arms
of the 'star' by converse movements (Fig. 157). Expansion of the pig-
ment masses of a given set of chromatophores gives their particular color
(or optical colors which they influence) to the skin region in which the
expansion occurs. The aggregation or contraction of the pigment masses
makes of them minute dark dots in a pallid expanse of skin, lightening
up the animal's coloration or giving some other class of chromatophores

526 ADAPTATIONS TO PHOTIC QUALITY

a chance to affect it by expanding. Both the expansion and the contrac-
tion of the pigment mass appear to be active processes — neither is com-
parable with the relaxation of a muscle.

Chromatophores are of several types. Most widespread of all is the
'melanophore', containing the dark brown, almost black pigment melanin.
The predominance of melanophores is largely responsible for the fact that
dermal changes of shade, in an achromatic sense, are more widespread
among species and more conspicuous in individuals than are changes of
hue. This predominance probably indicates antiquity. Other types of
chromatophores would seem to be newer inventions. Some of them oper-
ate quite differently from melanophores. In a particular species, one type
may be changeable and another not; and in some animals (lizards,
snakes) they are all quite inert so far as we can tell.

Some colored chromatophores, generically called lipophores because
their pigments are fat-soluble carotenoids, take their special names from
their colors : erythrophores (red) , xanthophores (yellow) , xantholeuco-
phores (changeable from yellow to white) and so on. A third class is
comprised by the iridocytes, which may be inert or active, free or associ-
ated closely with other chromatophores to form iridosomes. The pigment
in iridocytes is the familiar guanin, which may give the cell a white or sil-
very color, or even produce an enamel-like yellow, blue, or green depend-
ing upon the way in which the platelets of guanin operate to produce in-
terference between the wavelengths of light they reflect. A single iridocyte
may, as in Fundulus parvipinnis, scamper through green, orange, yellow,
and red phases in successive moments.

*PhysiologicaV and ^Morphological' Chromatophoral Changes

Chromatophoral changes may have little to do with illumination, or
they may closely adapt an animal to the shade of its surroundings, to the
color of the background, or to both. In some species (as certain flound-
ers) even the pattern can be roughly matched, as Sumner first showed
in 1911. The fishes take on large blotches when over a coarse polka-dot
pattern, small spots when on a small-dotted background. These rapid,
transitory changes (not of pattern, however) were of course known to
the ancients, and were described for the chameleon and invertebrates
(cephalopod molluscs) by Aristotle. As early as 1882 Flemming sug-
gested, on the basis of his experiments with salamander larvae, that the
actual number of chromatophores could be influenced by the surround-
ings of the animal. In 1909, Secerov coined some terms to express the
distinction which his work on a fish (Barbatula barbatula) led him to

CONTROL BY THE EYE 527

make : the quick changes he called 'physiological', the slower ones, requir-
ing weeks or months and having their basis in an increase of the amount
of pigment or the number of pigment cells, or both, he called 'morpho-
logical' color changes. These terms are not too good, for both kinds of
change are equally physiological phenomena; but they have stuck. The
very existence of morphological changes was questioned by reviewers right
up to 1928, but in the past decade evidence for them has been piled up.

In 1910-1913 Babak, working with salamander {Amby stoma) larvae,
came to a conclusion which is now known as Babak's law: If the con-
ditions for producing a given physiological color change are maintained
for a long period, the corresponding morphological change will take
place if it is within the capacity of the animal. Modern experiments,
especially those of Francis Sumner and his co-workers at the Scripps
Institution of Oceanography, tend to show that while Babak's law holds
pretty well, the relationship it expresses is not a genetic one. Morph-
ological changes are apparently not the direct result of the chromato-
phoral system's setting itself in a given state and holding that state —
rather, the two kinds of changes have a common cause.
Control Through the Eye — This cause is always an intricate one, and
varies from group to group of animals. Lister established in 1858 that in
the frog the eye initiates the process of dermal change, and we now know
that this is nearly always true. If the eyes of poikilochromic (/. e., color-
changing) vertebrates are covered or removed, no further responses to
background — or at most only slight ones — occur. Responses to temper-
ature, and to light and darkness, may however go on about as before.

The eye is thus not only the receptor for vision, and for a host of
reflexes concerned with its own control, but it also mediates a reflex arc
of some sort which ends in the dermal chromatophores. What constitutes
the middle of the arc- — whether nerve impulses or blood-borne substances
— is another matter. Before considering that matter, it needs pointing
out that for the eye to control dermal responses to its field of reception
has no implications whatever for vision in that field. We need not sup-
pose that for an animal to respond to a background, he must be visually
conscious of its characteristics of hue and tone. As a matter of fact, the
eye of a fish can adjust its melanophores to different neutral backgrounds
whose difference in tone is too small for the same fish to discriminate
visually in a training procedure! Of course in the work of Mast cited in
the preceding Section, the instant choice of a particular background by a
flounder adapted, dermally, to that background certainly had a basis in

528 ADAPTATIONS TO PHOTIC QUALITY

whatever visual consciousness a fish may possess. More recently Brown
and Thompson have shown that in eight species of freshwater fishes, in-
dividuals adapted to pale or dark backgrounds would prefer the respec-
tive backgrounds when allowed to make a choice. But the color changes
mediated through the eyes are just as mechanically reflex as is the visceral
disturbance we may experience from certain shifting patterns of visual
stimuli which we cannot even recognize or describe.
Physiological Color Changes in Teleosts — Of all fishes — indeed, of
all vertebrates — it is the teleosts which display the greatest versatility in
both physiological and morphological changes of costume. And, it is
these forms whose chromatophoral performances are most wholeheartedly
devoted to fitting the animal to the pattern of its surroundings. Many
marine forms, like the swordfish and tuna, do have relatively inert color-
ations. Very probably this is because, being pelagic, they are never near a
substrate or background and have no need of a capacity for adjusting
thereto. But many littoral fishes, particularly marine ones and especially
the hordes of tropical coral-reef species and the rock-reef fishes of the
temperate zones, can manipulate their colorations with real virtuosity,
and may match their backgrounds closely. The groupers (genus Epi-
nephelus) have been called the chameleons of the sea — which is a gross
under-compliment since the true chameleons actually have less of a
dermal repertoire than a tree-frog. Some of the flatfishes are not far be-
hind the coral-reef fishes. The rapidity of their shifts of color as they
glide over a variegated pattern has been called 'blush-like'. One Nassau
grouper in a New York aquarium was observed to don eight radically
different liveries within a period of a few minutes. Beebe has described
a fish which he watched as it swam in amongst some coral and out again.
When it went in, it was a shining blue with three vertical brown bands.
When it came out a few moments later it was a brilliant yellow, thickly
covered with black polka-dots — and Beebe was able to assure himself
that it was really the same fish.

There are species in which portions of the whole color pattern reside
in internal organs (peritoneum, meninges, etc.). These colorations show
through to the surface owing to the transparency of the overlying struc-
tures, and are blended with patches of dermal color to form the overall
pattern of the fish. This is the situation in Coryphopterus glaucofrcenum ;
but in Eviota personata all of the color pattern is internal, the muscles
and bones are transparent, and there is but little pigment in the skin.
These internal colorations change in sympathy with, and in cooperation

COLOR CHANGES IN TELEOSTS 529

with, the changes in the skin; but nothing is known concerning their
immediate causation and control.

Mode of Control in Teleosts — The speed with which fishes can effect
skin changes, together with the fact that they occur all over the body at
once, speaks for nerve impulses; and in fact it is now generally believed
that in all poikilochromic teleosts the nervous system is in practically
complete charge as lieutenant to the eye. The work of Pouchet in 1876
was the first to indicate this. The cutting of nerves in turbots put out of
action the chromatophores of corresponding skin areas. In 1893 Ball-
owitz demonstrated profuse nerve endings on the melanophores. Others
since have been able to make out that these autonomic fibers are of two
kinds, affording a double, reciprocal innervation. There is a little
evidence that endocrine secretions — so nearly all-important in amphibian
dermal changes — play a very minor part in teleosts. It has been claimed,
though with insufficient proof, that posterior-pituitary extracts increase
the amounts of melanin in teleost melanophores, and that the lipophores
have no nerve supply at all and are entirely under pituitary control. The
isolated melanophores of a single scale will respond to autonomomimetic
and other drugs (though not to visible light) , but this does not imply as
much for a hormonal control in the intact fish as it may seem to do. We
now know that nerve fibers arouse effector end-organs by means of sec-
retions from their tips — the so-called 'neurohumors' ; and that these latter
include such substances as adrenalin and acetylcholine. Nervous and
hormonal control-mechanisms may thus be said to have a common
denominator.

It has been found that depressants of the nervous system, such as
anaesthetics, produce an 'expansion' of the melanophores of Fundulus;
while reflex paling results from the administration of stimulant drugs.
The dermal changes of this much-studied fish are speeded up by increased
temperature, and proceed at different rates under the different osmotic
circumstances of fresh water versus salt; but these facts are not incom-
patible with the idea of nervous control. When a spinal nerve is cut, as
Pouchet originally showed, the melanophores in the skin supplied by the
nerve become expanded and remain so for many days, until the motor
fibers of the nerve regenerate. Some slight and sluggish activity remains
in the chromatophores however, even after their denervation, indicating
that the ebb and flow of hormonal concentrations in the blood stream
are not without some effect. Local interference with the circulation abol-
ishes this residual activity, though this may be due more to the shutting

530 ADAPTATIONS TO PHOTIC QUALITY

off of the oxygen supply than to a deprivation of hormonic stimulation.
More significant, and suggesting a direct chemical influence of the retina
itself, are the recent experiments of Szepsenwol. He transplanted the
adult eyes of Fitzroya lineata to new locations in the body where they
could have no connection with the nervous system, and found that the
chromatophores would still perform.

Response to Albedo — The physiological dermal changes of the aver-
age teleost consist of simple darkening on dark backgrounds and paling
on light or white ones. Both normal and eyeless animals become pale in
darkness, but eyeless animals mysteriously darken in the light. In some
species, as in the flounders lately examined by Osborn iPseudopleuro-
nectes americanus and Lophopsettd aquosa) , the blinded fish takes on
an intermediate shade, and the dark spots normal for the intact animal
disappear — this being the pattern which the intact fishes assume in dark-
ness.

It may seem odd enough that a blinded fish should respond to light at
all, and we will consider the possible reason for this in a page or two;
but there is an even greater peculiarity about the responses of the intact
fish to light and dark backgrounds : it was Sumner who, years ago, first
noticed that in these responses the intensity of illumination is of little
consequence. This has been abundantly confirmed since, and has always
seemed remarkable. If the fish were responding merely to the amount of
light entering the eye, it should give the same dermal response to a
brightly illuminated dark background as to a dimly illuminated white
one — which would not adapt the fish at all! Instead however, the shade
assumed by the skin of the fish is always (unless the intensity of the in-
cident light is very low or extremely high) in accordance with the albedo
of the substrate — the percentage of incident light which the substrate
reflects.

A response to albedo sounds impossible. It would be like a response
to specific gravity. The strange thing is that we do respond to specific
gravity — in the so-called size-weight illusion, wherein a pound of lead is
actually judged heavier than a pound of feathers. Analogous, also, is our
ability to recognize a melody as 'the same' after transposition to another
key.

These phenomena have their counterpart, in human vision, in the one
which psychologists call brightness constancy. We see snow as white in
the evening, and see coal as black in noonday sunlight, even though the

COLOR CHANGES IN TELEOSTS 531

coal may be reflecting more photic energy than the snow had done. In
some way, our perceptual machinery (not our thinking processes — it
works too fast for them to be involved) makes allowances for the intens-
ity of the general illumination. We can easily be led to see white paper
as gray, or black paper as nearly white, if our clues to the overhead illum-
ination are eliminated in an experimental situation. Similarly, the even
more fully automatic 'allowance-making' mechanism of the fish can be
deceived. If, by such devices as the use of translucent material lighted
from below, the substrate is made lighter or darker than the overhead
illumination would call for, the skin of the fish changes accordingly.

Sumner early suspected that this ability of the fish to adapt the chrom-
atophores to background albedo was due to a vertical polarization of the
retina. The retina was thought to control the pigment cells in sympathy
with the relative illuminations of its upper and lower halves, correspond-
ing respectively to the lower part of the visual field (the substrate) and
the upper part (the source of natural light) . Von Frisch soon produced
experimental evidence for this view, to which Sumner and others have
since added a great deal.

By means of vaseline-lampblack paint, and by fitting celloidin caps,
blackened in various patterns, over the corneas of fishes, Frisch and Sum-
ner have shown that when the upper half of the cornea is left clear and
the lower half blacked out, the fishes will darken greatly regardless of
the tone or albedo of the substrate. If only the lower cornea is clear, pale-
adapted fishes remain pale on either white backgrounds or dark gray
ones. All-black covers did not always prevent all shade-changing ability,
probably because light could still reach the retina through the translucent
tissues of the head. Ordinarily, however, fishes so provided darkened up
as though they were eyeless. In the entire situation, then, we can see
certain tendencies:

A. When no light is striking the fish (with or without its eyes), the
melanophores 'contract'.

B. When light strikes only the skin (whether the eyes are present or
not), the melanophores 'expand'.

C. If more of any light entering the eye strikes the upper part of the
retina, the melanophores 'contract' despite Tendency B.

D. If more of the light entering the eye strikes the lower part of the
retina, the inhibitory effect of Tendency C upon Tendency B is ineffec-
tive, and the melanophores 'expand'.

532 ADAPTATIONS TO PHOTIC QUALITY

Thus in the ocular control of dermal response to the shade of the
background, the upper half of the retina acts positively to contract the
chromatophores, and the lower half of the retina acts in a negative way
to prevent such contraction. A blinded fish darkens in the light because
there is no eye to inhibit the innate tendency of an illuminated melano-
phore to expand. In other words, C (above) becomes impossible.

Frisch found, in trout, that blacking out one eye led to a darkening of
only one side of the fish — the opposite side, because of the total decus-
sation of the optic nerve fibers in the chiasma (Fig. 21, p. 47). Sumner
did not find this response in the species with which he worked. A fish
with one eye covered took on a shade intermediate (for a given back-
ground) between a normal fish and one with both eyes covered. Either
eye ordinarily can control all of the melanophores, which seems to dem-
onstrate an interesting phase of binocularity in piscine ocular physiology :
despite the total decussation of the optic nerves, each retina has connec-
tion within the brain with both halves of the central nervous system. The
unilateral response in the trout (and other fishes) seems to be the best
kind of evidence for nervous control of the melanophores. No hormone
could very well remain only on one side of a vertebrate's body.

Various attempts to confirm and study the 'polarization' of the retina
by inverting the illumination, rotating the fish, or destroying either half
of the retina have been successful. Not so, most efforts to rotate the eye
of a fish 180° in its orbit without killing the animal. Butcher, however,
has succeeded with this operation in Fundulus, and finds that the fish
will then give its tawny response to a yellow background only when the
latter is above the animal.

In general, dermal responses to hue exhibit no polarization at all. That
is, no contrast between the upper and lower parts of the visual field is
required. This seems particularly interesting when one recalls the con-
tention of some workers, that the colored chromatophores of fishes are
not controlled through the nervous system. Sumner got the same yellow-
ing of his fishes when corneal caps were applied whose upper halves were
yellow, black, blue, or clear — so long as their lower halves, admitting the
light reflected from the white substrate, were yellow. With an all-red
covering, the fish took on the same dermal color as when in a red con-
tainer with its corneas naked.

Morphological Color Changes in Teleosts — At the present time it
is the morphological color changes which hold the stage of interest.
Occurring in the same directions of darkening and paling, under the

COLOR CHANGES IN TELEOSTS 533

same conditions as the evanescent physiological changes, their causational
chain of events is not yet wholly clear. They appear to be usually under
the ultimate control of the eye, though when flounders are illuminated
from below and proceed (after many months) to acquire active chrom-
atophores of all sorts on their erstwhile snow-white undersides, it is some-
times hard to see how the eyes could have been responsible. Not all flat-
fish species have their eyes raised on any sort of 'turrets', so that they
could possibly see the substrate. It is difficult to imagine how year-long
streams of nerve impulses can evoke chromatophores from the meso-
dermal nowhere, or cause them to vanish entirely. And, the increase in
the number of melanophores of an illuminated, eyeless, fish is as much
of a mystery as is the physiological darkening of such fishes by light.

The commonest morphological changes in teleosts occur outside of
laboratories. Aquarists have long fretted over the fact that some of their
most gorgeous prizes soon become drab in captivity. The loss of glamor
can often be forestalled by careful attention to the diet; for a goodly part
of dermal matching-of-environment is really quite automatic, due to the
fact that the fish acquires many of its pigments directly by eating the
flora and fauna of his immediate environment. To a certain extent, the
fish can't very well help taking in some of the very colors which surround
him!

When a fish is kept for a long time on a dark or black background,
the actual number of melanophores increases and the total amount of
melanin extractible from the fish (and, perhaps, per melanophore) also
increases. Concomitantly the guanophores decrease — at least, the amount
of extractible guanin is reduced. Kept for weeks on a white ground, the
fish will increase its guanin coating and will decrease the number of mel-
anophores. Just what happens to these we do not know, though Ogneff
thought they were phagocytized, eaten up by wandering tissue cells.

Blinded teleosts, and amphibians too, usually lose melanophores when
kept in the dark. This fact has been used to account for the absence of
dermal pigment in (permanent) cave-dwelling vertebrates, all of which
belong to these two classes. Eyed animals of course also become depig-
mented in darkness, but eyeless individuals do not remain pallid when
brought into the light. Their melanophores not only quickly expand,
but soon begin to increase in numbers — not, however, if the pituitary
gland is removed along with the eyes. Minus its pituitary, an eyed or
blinded fish proceeds to lose melanin. Hilton found that adult Typh-
logobius, which are normally eyeless and unpigmented (p. 388), would

534 ADAPTATIONS TO PHOTIC QUALITY

develop chromatophores on the head if kept in the light for several
months. Kurz has found that larval flatfishes (Pleuronectes) , placed in
the dark, cease to form any more melanophores and never develop lipo-
phores at all. He also found that in these fishes (but not in the pike,
Esox) white and short-wave lights stimulated the development of all the
pigments while red, yellow, and green lights retarded them.

Abramowitz has reported that in Fundulus majalis the number of
xanthophores increases within two to six weeks when the fish is kept over
yellow or black substrates, decreases when the animal is over blue or
white grounds. Sumner and Fox, however, found that in Girella the
amount of xanthophyll extractible was greater in black individuals from
black surroundings than from yellow fishes assayed after a sojourn on
yellow or gray. Actually, there had been no gain in xanthophyll in the
black fishes — only less of the loss which in Girella ordinarily occurs in
the laboratory anyway. However, some of Sumner's recent work has in-
dicated that fishes can deposit more xanthophyll in the skin than is
accounted for in the food supplied to them. This hint, that fishes can
convert carotene into xanthophyll, is borne out by the work of Lonnberg
on Swedish marine fishes. Lonnberg finds only xanthophylls, no caro-
tenes, in the skins of certain fishes which feed upon crustaceans lacking
xanthophyll (but possessing carotenes) in their own pigmentations.

As with his demonstration of the response to albedo in physiological
adaptation to substrate tone, so also Sumner has found an analogy for a
visual phenomenon at work in the morphological changes of teleosts. In
Gillichthys, Gambusia, and Lebistes, counts of the number of melano-
phores per unit area, or determinations of the amount of melanin in the
skin, showed that the increase of pigmentation was inversely related to
the logarithm of the albedo of the substrate. It was not surprising that
the albedo should prove so important, and the intensity of the incident
light a minor consideration; but the mathematical character of the relat-
ionship was unexpected.

Sumner has advanced the suggestion that this aspect of the morph-
ological changes is in line with Fechner's modification of 'Weber's law'.
The latter is a battered old psychological dictum to the effect that if, in
any sensory modality, two stimuli differ quantitatively just enough to be
perceived as different, their objective difference expressed in per cent is a
constant. For example, if a five-pound weight and a six-pound one can
just be told apart by heft, one is 20% heavier than the other, and any
two weights must then differ by 20% to be discriminable. Fechner be-

COLOR CHANGES IN AMPHIBIANS 535

lieved that the threshold of difference was not a constant percentage in-
crement, but rather that it varied as the logarithm of the magnitude of
the stimulus.

In psychological phenomena, Fechner's (or Weber's) law breaks down
with both high and low values of the stimulus, but holds fairly well for
a long intermediate range of values. So, Sumner finds, does the log-
arithmic relationship of increased pigmentation and albedo. Whether or
not this phenomenon is an instance of the operation of Fechner's law, it
is difficult to say. But when the control of the adaptive alteration of the
protective colorations of vertebrates was originally delegated, logically
enough, to the eye, it was also fairly logical that the eye should proceed
to administer this particular physiological territory in accordance with
the laws governing its own operation as the receptor of the visual sense
— even though visual consciousness plays no part in the processes of
color-change control.

Color Changes in Amphibians — Lister's pioneer work suggested that
the dermal changes of the Amphibia are nervous reflexes. This idea was
supported by Babak in 1910-1913, and in fact was quite generally accept-
ed up to about 1924. The physiological changes of a frog between its
pale and dark phases may take hours, or a day or more, to accomplish.
In some tree-frogs, a few seconds may suffice. Morphological changes
can be induced by experimental illuminations, and are particularly sus-
ceptible to dietary manipulation. These changes are of course a matter
of weeks or months, as in teleosts. Such slow actions hardly look like per-
formances of the nervous system. Yet if the eyes are removed, or the op-
tic nerve cut, the changes in response to illumination are largely inhibited.

In 1898, Corona and Moroni found that injections of adrenal extracts
would blanch a frog. Lieben rediscovered this reaction eight years later;
and from 1922 on, Hogben and his colleagues argued for an almost
strictly hormonal intermediation between the eye and the 'pigmentary
effector system' of amphibians. As long as adrenalin was the only endo-
crine substance known to affect the phenomena, there was still room for
the nervous system as the centerpiece of the picture; for the association
of the adrenals with the sympathetic nervous system was well established.

But Hogben found that extracts of the intermediate lobe of the pitu-
itary would darken frogs; and he came to believe, from further experi-
ments, that a blanching hormone was produced by the pars tuberalis of
the same gland. Much of this work was done on the primitive African
clawed frog, Xenopus Icevis. In this country the studies of Parker and

536 ADAPTATIONS TO PHOTIC QUALITY

Others on the local Rana pipiens indicate that in this frog only one pitu-
itary hormone is involved, not two. Blood serum from dark pipiens, in-
jected into pale ones, will darken the latter; but interestingly enough
pale-frog serum fails to blanch dark frogs. Adrenalin injections, or the
removal of the pituitary, will produce a more complete paling than will
the bright illumination of a normal frog in white surroundings. Frogs
whose pituitaries have been removed will, in time, lose much of their pig-
ment— a 'morphological' change. Experiments similar to those of Szep-
senwol (p. 530), designed to test whether the eye itself secretes skin-con-
trolling hormones, have yielded conflicting evidence in amphibians.

In amphibians the color-changes are less widespread and conspicuous,
as well as less rapid, than in teleosts. Few have any greater repertoire
than the brown-green-cream series of phases in the common tree-frog
Hyld yersicolor. Not only is the control largely (sometimes, wholly)
hormonal instead of predominantly nervous (except in a few tree-frogs) ,
but the authority of the eye has begun to dwindle, approaching the situ-
ation in lizards. In some forms, as for instance the common newt
{Tritums riridescens) , the pattern of the adult shows no measurable
changes toward photic stimuli, though darkening will occur at low tem-
peratures and paling can be induced by pituitrin. Response to back-
ground does occur in many species, but only when temperature and hum-
idity conditions permit — a conjunction which is so far from being the
rule that it is almost an accident. When a frog is caught in the daytime
amid green grass, and happens to be green in color, it is in a sense a coin-
cidence. At a lower temperature, the frog would have been brown. So
also, if the grass had happened to be wetter. The frog can blend with its
environment only when three factors are just right: light, temperature,
and moisture. The eye can aid the response to only one of these factors,
/. €., light. In teleosts, the eye is able to control the skin largely because
temperature and humidity do not control it. But at least amphibians are
able to attain the pale phase (appropriate to bright light and backgrounds
of high albedo) at moderate temperatures — in contrast to the situation
in most lizards, which can take on their pale phases only at relatively
high temperatures.

Even tactile stimuli may have an influence. The European tree-frog,
ceteris paribus, will turn brown on a rough surface and green on a
smooth one. In a roundabout way, such changes are perhaps adaptive to
background, for the brown bark of a tree is rough, and the green leaves
are smooth.

LOWER FISHES; DIURNAL RHYTHMS 537

In still other ways, the amphibian phenomena differ from those of
teleosts. Blinded frogs, like normal ones, respond dermally quite inde-
pendently of light and darkness in situations which are warm and dry or
cold and wet. At moderate temperatures, in the presence of adequate
moisture, the melanophores of eyed frogs contract in bright light and
expand over dark backgrounds. But in darkness they also expand, instead
of contracting as in fishes. Blinded frogs expand their melanophores in
darkness, and these will contract only to a tiny extent if the animals are
then illuminated. However, Laurens found that in larvae {Amby stoma)
the reactions of blinded individuals were like those of blinded teleosts,
though markedly retarded as compared with normal larvae. The primitive
tendency of melanophores (as shown in teleosts and in young amphibian
larvae) is, as Parker has pointed out, to expand in the light and contract
in the dark. With age, the eye comes to be able to inhibit the expansion
in the light; and, in amphibians, the presence of the eye — if in its normal
location, at least — somehow causes or permits the melanophores to ex-
pand in the dark.

By and large, the dermal color-changes of amphibians are nowhere
nearly so clearly adaptive to background as those of teleosts. This is even
more true of the lizards. Darkening in low temperatures, and blanching
at higher ones, are such predominant activities that Max Weber was
prompted years ago to suggest that in both amphibians and reptiles the
dermal changes are designed primarily to regulate the temperature of the
animal, by adjusting the light-absorbing capacity of the skin. We will
consider this theory shortly when we come to the reptiles.

Dermal Changes in Lower Fishes, and 'Diurnal Rhythms' — The

seemingly paradoxical physiological kinship of the Amphibia and the
elasmobranch fishes, manifested in various other ways, is also borne out
by the character of color-change control. Color changes in elasmobranchs
went unnoticed until less than a decade ago. These fishes are generally
grayish or neutral in garb; and though they are sometimes stated to have
no typical melanophores, they are capable of changes in shade. The eye
operates these changes by way of the pituitary in all the investigated
species except one, wherein the blanching process (though not the dark-
ening) seems to be under the direct control of the nervous system. No
morphological changes are known to take place in elasmobranchs.

We do not know much about color changes in other 'lower' fishes. At
least two of the three lungfishes (Protopterus and Lepidosiren) have
them, but their operation has not been investigated. In 1935 Young

538 ADAPTATIONS TO PHOTIC QUALITY

found that in lampreys (Lampetra) , the dermal changes are mediated
through the pituitary and not through spinal nerves, and that the median
eyes (see p. 339) share in the control of the changes, along with the
lateral eyes.

Lampreys, Young found, become paler at night, darkening in the
daytime — and keep up these changes for many days when kept in con-
stant darkness. Similar intrinsically rhythmic changes were reported in
1926, by Pauli, for a teleost {Phoxinus) , where they were very slight,
and for larvae of Salamandra maculosa, in which they persisted for about
a week. Slome and Hogben, in 1929, reported marked rhythmical
changes in an anuran (Xenopus Icevis) kept in the dark.

Such diurnal rhythms, which occur also in the retinal pigment cells of
some fishes (perhaps also in frogs) , are inherent, and outside of the con-
trol of the coloration by the photic stimulation of the eyes. Whatever
their cause, it is suppressed by light. No vertebrate exhibits any rhythm-
ical dermal changes when kept illuminated night and day.
Color Changes in Reptiles — Despite the reputation of the chameleon
for being able to match any colored background (and its alleged tend-
ency to suicide when placed upon plaids) , it can be asserted that no rep-
tile dynamically adapts its skin primarily to the background. The dermal
response to the character of the light entering the eye, or to bright light
in bright surroundings, may suit the animal's pattern better to the back-
ground; but any such improvements of concealment are even more com-
pletely fortuitous than they are in amphibians.

It is only in lizards that conspicuous changes occur. Even among the
lizards there are only a few families which show chromatophoral changes
well — notably the Agamidas of the Old World and their counterparts,
the Iguanidae, in the Western Hemisphere; and of course the Chame-
leontidae. The only changeable pigment cells are the melanophores, which
in most reptiles underlie the iridocytes but, in poikilochromic forms, send
the pigment up into cell-branches which are intertwined with the vari-
colored iridocytes.

To no lizard has the color of the background any significance. A
response to hue is made in a curiously indirect way, however, by Anolis
carolinemis, the 'Florida chameleon' (which is really an iguanid). Re-
sponses to light and darkness by paling and darkening are about as in
the teleosts, but they are even more at the mercy of temperature changes
than in amphibians. Each individual lizard has a light phase and a dark
phase. Wherever a species seems to have a great variety of costumes (as

COLOR CHANGES IN REPTILES 539

in true chameleons) it is due to individual variation. Thus particular
chameleons of a single species may vary, in their pale and dark phases,
between green and dark brown, yellow and olive, buff and black, etc.

The melanophores react to temperature as in the amphibians, expand-
ing at low temperatures and contracting in high ones. In general, while
contraction will occur in amphibians at average outdoor temperatures, in
lizards the temperature must be rather higher before paling ensues even
in bright light. If the lizard happens to be a desert form and, after paling
in the heat of the sun, blends fairly well with the sand, we may call this
adaptation to background if we stretch a point. Actually however, Max
Weber's idea seems pretty sound where lizards are concerned. By paling
at high temperatures (which ordinarily means in the sun) , and darken-
ing at lower ones, they can reflect light (and heat) when they are already
well warmed, and absorb a larger proportion of it when the absolute
amount available is less. No useful purpose, in connection with heat-con-
servation or anything else, seems to be served by the paling which takes
place in darkness, however. Here, probably the ancient proclivity of
melanophores to contract in the dark is only asserting itself, and we need
not seek any ulterior explanation.

The lizard's responses to high and low temperatures are direct re-
actions to temperature. But we may, if we like, take the attitude that
they are biologically intended, so to say, as responses to the accom-
panying light and darkness : bright light, in the environment of a lizard,
means high temperature; dim light or darkness connotes the cooling of
twilight and nightfall. Here we have an analogy for the effect of sub-
strate texture upon the European tree-frog (r. s.).

Light and darkness, as such, are effective only within a restricted
range of temperature. Within this range, the similarity of the behavior
of lacertilian and teleostean melanophores is striking, as Sand pointed
out a few years ago. They contract on white backgrounds and expand
on black; they contract in darkness in both normal and eyeless animals;
they expand in eyeless animals upon illumination of the body; and they
expand in any denervated area of the skin. Blindfolded animals, unlike
eyeless ones, remain dark upon lighted backgrounds, showing some in-
hibitory influence of the eye ; but this influence is readily masked by that
of temperature or excitement.

The response to denervation is but one of a number of indications
that the eye exerts its control through the nervous system. The responses
to temperature, however, are of doubtful mediation. Like those to light,

540 ADAPTATIONS TO PHOTIC QUALITY

they go fast enough to make nervous control seem reasonable — much
more so than in most amphibians. The consensus, however, is that in
lizards the principal controlling mechanism is an antagonism between
adrenalin and a dispersing hormone produced by the pars intermedia
of the pituitary.

The response to excitement is particularly prompt, but it is unques-
tionably entirely endocrine. This response is given by lizards to any noxi-
ous stimulus, a number of which — electrical stimulation of the mucous
membranes, for example — are used experimentally to induce the so-
called excitement pallor. Its appearance is very regular, but may be sup-
pressed by low temperatures. The blanching has been abundantly proven
to be brought about by the adrenals. It occurs even in denervated areas,
indicating that the influence of adrenalin is direct, and that the adrenalin
or adrenalin-like substance involved is not a neurohumor, secreted in tiny
amounts by nerve fibers ending in the chromatophores. Hadley, however,
doubts the direct action, on the basis of his 1931 experiments on bits of
excised Anolis skin. While the melanophores of such bits would respond
directly to illumination, showing them to be apparently normal despite
their isolation, direct applications of strong adrenalin expanded them —
whereas the same solution injected into an intact animal produced the
usual wholesale contraction and pallor. Pituitrin expanded the pigment
cells both in intact lizards and bits of skin.

Local effects have also been produced in the intact animal. Redfield,
working with the horned lizard Phrynosoma, found that local heating of
the skin (light being excluded) would contract the melanophores without
affecting those elsewhere. Local illumination is also effective as a stim-
ulus, but produces expansion — which cannot here be due, like so many
supposed biological effects of light, to a heating action of the light. But
this apparently paradoxical expansive effect of heatless light does tie
in with some of the findings of Sarah Atsatt, whose recent paper on
desert lizards may sometime be called a classic :

Miss Atsatt so designed her apparatus as to divorce temperature from
light, and make each independently variable. Her findings tend to ex-
plode some hitherto well-rooted ideas, but they were so different for dif-
ferent species that only further work along the same line will show just
which of our smug generalizations (some of them stated above) must be
discarded. In thirteen iguanid species and one gecko, the response to high
temperature (35-43 °C) was the light phase; and to low temperature, the
dark phase. One species, Callosaurus rentralis, became partly pale again

COLOR CHANGES IN REPTILES 541

quite regularly, as an afterthought, after some time in low temperature.
Among the forms she studied, the one which was most active in the
winter was Uta stansburiana stejnegeri; and this species took on its pale
phase at a temperature as low as 25 °C — a behavior comparable with that
of amphibians.

Seven of the iguanids became pale in darkness and dark in the light
(at moderate temperatures) but five species showed no differences in
light and darkness, being obedient only to temperature. Two species of
Xantusid available to Miss Atsatt responded to both light and high tem-
perature with the dark, phase, and would not take on the pale phase con-
sistently in either low temperature or darkness. In the light of the noc-
turnality of Xantusid, we might cudgel our brains for an interpretation
of this pecuUarity — except for the fact that Miss Atsatt's one gekkonid
species, Coleonyx variegatus, is just as nocturnal, and yet becomes pale
in high temperature and in darkness, and darkens in low temperatures
and in illumination.

An influence of hue upon the dermal responses of a lizard {Anolis
carolinensis) has been shown by the interesting preliminary experiments
of Wilson. This Tlorida chameleon' is the little chap sold at circuses,
with the disastrous advice to feed it on sugar-water. It is usually hawked
while tied to a board covered with green baize, and the pitchman is care-
ful to keep in the shade — else the animals cease to 'match' the board, and
turn brown. This is the whole gamut of the animal's changes — from green
to brown; but it does truly equal that of its African namesake.

Wilson fitted green cellophane covers over the eyes of the lizards, and
covered some glass jars with similar material. He found that the green
phase was always produced by darkness, the brown phase by bright light.
Any brown individual, placed in a green jar, became green. Green cello-
phane over the eyes induced the green phase. If the eyes were blacked
out, either white or green light induced the brown phase. If one eye was
covered with green cellophane and the other with black, the green phase
was assumed as perfectly as if both eyes were acting. A few animals with
green hoods, and in a green jar, became intemiediate in phase (yellowish
brown) ; but Wilson noticed that they seemed sluggish and were blink-
ing their eyes — hence it was only natural that they should be intermedi-
ate between the expected green phase and the brown one which they
would assume upon closing the eyes for an even greater part of the time
with the body exposed to light.

542 ADAPTATIONS TO PHOTIC QUALITY

These fascinating results help to explain why this lizard, which can
turn green and disappear when it is on a background of foliage in its
native haunts, does not always do so. Green light can stimulate the retina
to evoke, through the nervous system, a green body coloration; but any
light — even a green one — striking the body strongly, only leads to melan-
ophore expansion and the onset of the non-adaptive brown phase. If
there are any photoreceptors in the skin, they are unfortunately not
specifically responsive to green light.

Wilson points out that when Anolis is among leaves and the eyes
receive light filtered by other green leaves overhead, the green phase
ensues. The animal is then adapted to its background — though not, as a
teleost would be, through the character of the light reflected from that
background. But let the lizard come out from cover, still standing on a
green leaf, and the reception of light on its skin quickly turns it brown
and causes it to stand forth like the proverbial sore thumb. Despite the
interesting demonstration of a specific response of the oculodermal mech-
anism to green light, it seems over-charitable to credit this one reptilian
species with an adaptability to background in the teleostean sense of the
expression.

Color-changes have been reported in snakes from time to time; but,
apart from some authoritative-looking old claims by Leydig for Matrix
natrix, it is probable that all gross changes (particularly those in green
tree-snakes mentioned by Fuchs) are caused not by chromatophoral alter-
ations but by a spreading of the skin, revealing areas between the scales.
Dryophis, in the anterior part of the body, exhibits a startling change of
this character when excited.

Very recently Rahn has demonstrated that the dermal and epidermal
melanophores of rattlesnakes, and the epidermal melanophores in three
colubrid genera, will contract permanently if the pars intermedia (or the
whole pituitary) is removed. Injections of 'intermedin' expand the
chromatophores once more. Whether light and temperature alter the
skin color in any of these snakes (by way of the eye or otherwise) is not
known; but it is unlikely, inasmuch as the superficial layers of the epi-
dermis— those due to be shed at the next ecdisis — contain a pattern of
motionless pigment which conceals the activity of the melanophores be-
neath. The paling of the body, produced by removal of the pituitary,
manifests itself only after the next subsequent moult.

The only other reptile in which melanophore activity has been dem-
onstrated is the alligator. Kleinholz has found that the pigment in scat-

COLORATION OF THE EYE ITSELF 543

tered cells on the under surface of young specimens expands on black
backgrounds and contracts on white ones. Pituitary and adrenal extracts
respectively produce the same changes in the cells. It does not appear,
however, that these phenomena can have any biological value — they do
not occur on the visible parts of the animal, and may be absent in older
individuals. The long-standing noctumality of the crocodilians seems to
account well enough for the vestigial condition of their color-changes.
It may seem more surprising that the snakes, with such close taxonomic
and ecological affinities with the lizards, should show so little evidence
of dynamic adaptation to their surroundings. But this explains itself
when it is considered as a part of the evidence for a lengthy subterranean
sojourn of the earliest ophidians* (see Chapter 16, section D).

(C) Coloration of the Eye

Basis of Iris Colors — The color of the eye itself presents some interest-
ing problems — histological, optical, and ecological. Ordinarily, only the
iris is involved. The pigment of the iris epithelium may be the only color-
ing matter present (p. 16), but nearly always there are stromal pigment
cells containing various amounts of melanin, colored oils (iridocytes) , or
guanin and related substances which yield metallic appearances of silver,
gold, or colors. As often as not, the coloration of an iris is the resultant
of both pigmentary factors and such optical phenomena as interference.
A vivid color may result from the absorption, by superficial layers, of
some wavelengths and the differential reflection, by underlying tissues,
of only certain ones of the remaining wavelengths. In this way, the green
spots of a frog's skin and the blue iris of a Siamese cat are produced,
without respective green and blue pigments being present at all.

Possible Significance — In our thinking about the possible meanings of
eye colors, it is important to distinguish between pigmentation and color-
ation— these terms having respectively quantitative and qualitative con-
notations. Clearly, it is necessary for the pigments of an iris to absorb or
reflect the greater part of the total illumination striking it. Bright pig-
ments may contribute as much (or more) to the opacity of an iris, by
reflection, as dark pigments do by absorption. But the pattern of colors
the iris presents to the outside world is largely independent of the reflec-
tion-coefficients, or the amounts, of the pigments present. In short, a
given blue iris may reflect the same amount of light as a given red one.
Why, then, should one animal have the blue, and another, the red?

544 ADAPTATIONS TO PHOTIC QUALITY

Apart from the possible mirror-action of silvery fish irides (see p. 238),
there is no conceivable way in which the coloration of the iris can affect
the vision of the animal, except perhaps at the very border of the pupil
where the presence of brightly reflective material should theoretically
be detrimental (though a metallic ring at the pupil's edge is extremely
common in the lower vertebrates!). If iris colors in general have any
explanations, these must be in terms of the interpretations offered for the
body colorations of animals. A given iris pattern, then, might: (a) be
intended to conceal the eye; (^) be intended to make the eye conspicu-
ous; or (c) mean little or nothing.

Conspicuousness of the Eye — Many a writer on the subject of the
adaptive coloration of animals has dwelt upon the conspicuousness of the
eye and the means employed to abolish it. Three things tend to make the
eye stand out on an animal, so that potential prey and enemies may dis-
cover the animal by noticing its eyes, even though the rest of the body
may be well camouflaged. These three things are: (a) its roundness;
(b) the blackness and roundness of the pupil; and (c) its glisten, due to
its wetness.

Cott's clever drawing, reproduced here as Figure 158, shows strikingly
how a round object set among other, even larger (but irregular) objects,
takes the attention of the beholder. A species of animal may so arrange
its coloration that the roundness of the eye is concealed. It is even poss-
ible to do something about the roundness and blackness of the pupil. But
there is no conceivable way of eliminating the glistening of the cornea —
though it eliminates itself under water, of course, in aquatic and amphi-
bious forms. All three of these causes of conspicuousness, it is interest-
ing to note, are employed in the 'warning' false eye-spots seen on the
wings and elytra of many insects, and also in fishes (e.g., Chelmon
rostratus) and toads ie. g., Mantipus ocellatus). Such spots are round,
black-centered, and are often even high-lighted to give the appearance of
glistening.

Concealment of the Eye? — The enthusiasts {e.g., Cott) say that the
color of the iris often matches that of the head as a whole. This is true
enough, and yet it is no evidence for a concealment function; for, aside
from the coincidence of silvery irides and silvery skins in many fishes, it
is true only of nocturnal and crepuscular vertebrates, and not of all of
them by any means. The crocodilians, for example, all have conspicuous
buff or yellow eyes, and yet their bodies are very dark or even black.

POSSIBLE VALUE OF EYE COLORATION 545

The strongly nocturnal oil-bird iSteatornis) has bright blue eyes, and
most owls have yellow ones.* Most wild mammals are dark brown or dark
gray, and their irides are almost always of some shade of brown — small
felids being quite exceptional with their metallic green. Under scotopic
conditions, favored by most mammals, it will not matter a particle, for
the concealment of the eye, whether the iris matches the body in color or
not, so long as the two are roughly matched in tone or albedo. But the
same, standard, dark brown mammahan iris occurs also in light gray

Fig. 158 — "Diagram illustrating the in-
herent conspicuousness of an eye-spot,
which attracts attention to itself in pref-
erence to a variety of other, and even
larger, objects in the visual field" (Cott).

Fig. 159 — Eye-masks. After Cott.

a, Oxybelis acuminatus.

b, Rana sphenocephala.

diurnal monkeys and squirrels — which is reason enough for thinking that
the dark iris of a dusky and nocturnal mammal has no standing as an
adaptation for concealment. Again, most salamanders have dark brown
eyes, yet many of them have gaily colored bodies.

Among those vertebrates which are much out where other animals can
get a good look at them — that is, the diurnal and arhythmic ones — it is
highly exceptional for the iris to be unicolor, and a match for the head

*So also the nortumal bat-eating hawk, Machaerhamphus alcinus.

546 ADAPTATIONS TO PHOTIC QUALITY

skin. In birds and lizards, particularly, there seems to be rather a ten-
dency to make the eye as contrasty as possible, and to employ it as a
decoration! But some representatives of nearly every class of vertebrates
bear markings which are supposed to be intended to conceal the eye :

These are such things as 'masks' and stripes of the head pattern which
continue unbroken across the conjunctiva and iris (Fig. 159). The eye-
masks of some fishes, frogs, and snakes are wide dark stripes passing
horizontally (or, in fishes, about as often vertically) across the eye, which
then loses its roundness since it is wholly 'absorbed' into the stripe. The
mask may not include all of the eye; but if the pupil is included within
its border, it is believed to serve just as well. Some masks are certainly
fortuitous — for instance, Cott figures an antelope which has a black
cheek-stripe sweeping up through the eye. Since a similar stripe develops
from the eye through the crumen to the jaw in an adult Hampshire
sheep (where it cannot possibly have any adaptive significance) such
markings in mammals must be viewed with suspicion from our present
standpoint.

More convincing, by far, are the instances where several fine stripes in
the head coloration pass unbroken over the conjunctiva and iris. Unfor-
tunately for any general acceptance of eye-concealment, such cases of
so-called coincident disruptive coloration of the eye are excessively rare.
Really good ones are such teleosts as Pterois volitans, Labrisomus nuchi-
pinnis, Ogcocephalus cubifrons, and Scorpcena plumieri; and young
specimens of our common painted turtles (genus Chrysemys), in which
several black and yellow lines cross the eye (Fig. 160), The pattern in
Chrysemys is closely imitated by that in the teleost Apogon maculatus.
Ida Mann noted a similar situation in one other turtle (Clemmys cos-
pica) and in one newt, Triturus torosus; but both of these examples are
inferior to Chrysemys.

It is claimed that the goatsuckers and frogmouths (and a couple of
lizards) close the eyes almost completely, as a means of concealing them,
when danger threatens. This action might also be expected in their close
relatives, the owls — who have so much more to conceal, since their irides,
though sometimes black, are most often a vivid yellow or orange.* But

*In one — Athene noctua — such a performance would only make the eye more conspicuous;
for, though this owl has yellow irides, it has white lids. In the daytime, owls have their
eyes closed (to conceal them? — or in sleep?) particularly when danger is not threatening.
The usual daytime photograph of an owl shows the eyes wide open, but this is because the
photographer has disturbed the bird. A truly natural picture of an owl huddled against a
tree-trunk (in its 'hiding' posture) always shows the eyes closed.

POSSIBLE VALUE OF EYE COLORATION

the owls do not have the habit. The narrowing of the lids in an emer-
gency is open to an utterly different interpretation: it may well be a
device for momentarily sharpening vision to a maximum, by employing
the lid opening as a stenopaic slit. Myopic humans do the same trick —
indeed, the very word 'myopia' is derived from roots which mean 'to shut
the eye'.

Related to the above matter is another claim of the enthusiasts: that
the best cases of eye camouflage, by masks and stripes, are seen in lidless
vertebrates. Pterois is lidless; but Chrysemys is not. But this and othet
turtles, Triturus torosus, fishes, and snakes do have something in com-
mon to which attention has not been called. The eyes of aquatic fomis,
lidless or not, have no glisten when under water; and the snake spectacle

Fig. 160 — Coincident disruptive coloration of the iris, conjunrtiva, lids
and surrounding skin.

a, head of a lionfish, Pterois voUtans. After Cott.
Chrysemys picta marginata; drawn from life.

b, head of the western painted turtle,

is SO quickly dulled after a shed that the snake eye seldom has the luster
of that of a bird or mammal. It may not be lidlessness as such, but the
absence of glisten, which has made it worth-while for these particular
vertebrates to devise camouflage for their eyes.

Glistening eyes, on the other hand, simply cannot be successfully con-
cealed. It almost seems as though the birds and lizards, realizing this,
have gone to the other extreme and have deliberately used the eye as the
centerpiece of their fanciest decorations. Consider the guano cormorant,
Phalacrocorax bougainvillii — it has a sober brown iris, but the naked
skin around the eye bears a green ring next the eye, and a red ring out-

548 ADAPTATIONS TO PHOTIC QUALITY

side of that. The proponents of adaptive coloration do not tell us why
so many species of vertebrates — fishes, lizards, and birds with bright-
colored irides; anurans, lizards, and cats with metallic ones — should
advertise their eyes, particularly when so many of these very same ani-
mals have their bodies 'concealingly' colored. The nocturnal animals on
which cats and owls prey do not, of course, see their enemies' irides as
colored ; but even so, the green of the cat's eye and the lemon iris of the
owl would assuredly be seen as light-toned spots, even by an animal
whose own vision was completely achromatic.

The difficulty of concealing the little black eyes in transparent fish
larvae has been discussed previously (see pp. 237-8). Partial success may
be attained by a precocious development of the silvery argentea layer of
the chorioid, just within the transparent sclerotic envelope. A situation
in one genus of batfishes, Lophiomus, to which Dr. Hubbs has called
the writer's attention, serves to emphasize most strikingly the fact that
the eyes of baby fishes often serve as a label, saying all too plainly:
"Here is food." The batfishes are related to the anglers, and like the
latter they are flattened dorsoventrally, with cavernous mouths over
which, in the various species, there are suspended various sorts and sizes
of 'illicia', or baits. The illicium dangles from a fishpole, rooted on the
animal's back, and serves to lure small fishes within reach of the maw
beneath it. In Lophiomus, the illicium takes the form of a translucent
fish larva — complete with a pair of beady black 'eyes' at the 'head' end.

Concealment of the Pupil? — The roundness and blackness of the
pupil are concealed well enough when the iris as a whole is dark in color
— though hiding the pupil in the iris only means that the whole iris is
now as hard to hide as a pupil of the same size. In many fishes a thin
black stripe, no wider than the pupil, may contain and absorb the latter.
Such cases are enormously outnumbered, however, by those in which the
pupil is rendered conspicuous or made to appear larger than it really is :
No more conspicuous pupils exist than those of most fishes, since the
irides of most fishes are silvery. In birds, the iris may be dark brown
(most passerines) ; but it may also be yellow, blue, green, etc. and these
colors may contrast vividly with those of the feathers. Where the iris is
brightly colored, the eye itself is rendered conspicuous and at the same
time the pupil is rendered doubly so. This latter point may be dismissed
as accidental; but not so the many instances among lizards, where not
only is the range of iris colors greater than in birds, but even forms with

POSSIBLE VALUE OF EYE COLORATION 549

dark irides have these flecked with metaUic pigments, making a quite
gratuitous contrast with the black of the pupil. The common frogs, and
many fishes and birds have the pupil outlined by a thin gold or silver
line, the rest of the iris being so dark that the pupil would be beautifully
concealed in it were it not for this metallic frame. To the adaptive color-
ationists, putting this ring around the pupil must seem about as mean a
trick as hanging a bell on a cat.

In many diurnal snakes, particularly those of the racer type, a black
blotch on the nasad part of the iris comes right to the edge of the pupil,
which is otherwise bordered by a C-shaped metallic line. Thus the pupil
appears egg-shaped, and nearly double its true area. If the gap in the C
(which occurs just where the important forward-looking line of sight
passes the pupil margin) exists to prevent distortion of the retinal image
through diffraction at the border of the metallic pigment, then we have
here an instance in which a very minor improvement in vision takes pre-
cedence over all considerations of iris-decoration for pupil-concealment.

One can only conclude that few animals have even apparently made
any effort to conceal the pupil; and that great numbers, which could
easily have made the pupil to blend with the iris, have 'spoiled it' by giv-
ing the pupil a false size, or a conspicuous outline, which serves no dis-
cernible purpose. Here, as with the eye as a whole, it is likely that the
conspicuousness produced by glisten is so great that the animals have
found it quite impossible to counteract the shininess by any sort of cam-
ouflage.

Sexual and Temporal Differences — Further indications of the gen-
eral meaninglessness of eye colorations are seen in the species showing
sexual dimorphism, and in those which have a capacity for changing the
color of the iris from time to time. If eye colors are concealing, we should
expect that if a few animals can change those colors, great numbers of
others could and would do so. We might expect to find animals, even
furred and feathered ones, blending their eyes into various backgrounds
just as a flounder, by dermal color-changes, suits its whole body (except
the eyes!) to the substrate. The chromatophores of the iris look enough
like those which alter the skin pattern so that one wonders why they
should not, as readily, alter the coloration of the iris.

Outside of the birds, there are but few animals which show a sexual
difference in eye color. In the common adder of Europe, Vipera berus,
the brown-and-black female has a light brown iris, while that of the gray-
and-black male is red — a most unusual color for any iris to have, outside

550 ADAPTATIONS TO PHOTIC QUALITY

of the fishes (where it is not uncommon, as for instance in the cen-
trarchids). In our common box turtle (Testudo Carolina) also, the male
usually has a red iris and the female a yellowish or brownish one. These
reptiles are such splendid examples of 'disruptive coloration' — as to their
bodies — that they force one to believe not only that their eye colors are
meaningless (in view of the colors themselves and the sexual difference)
but that if they could have camouflaged their glistening eyes they would
probably have done so.

There may even be great sexual differences in the apparent size, and
hence conspicuousness, of the pupil — as in the boobies (see p. 226).
Certain subspecific differences, like sexual ones, likewise suggest that eye
colors mean little or nothing. For example, one subspecies ikohnii) of a
certain terrapin {Graptemys pseudogeographica) has a most startling
snow-white iris.

Most remarkable — and meaningless — of all differences are the tem-
poral ones. The iris of a newborn human baby lacks stromal pigment
and is consequently blue (p. 16) — even in a negro. Other primates show
similar changes with age — the young Indri, for example, has greenish
eyes while the adult has light brown ones. Deepening with age is partic-
ularly noticeable in the pigmentation of the iris of the domestic cat,
which, like man, is always bom with blue eyes. In some species of birds,
the color of the iris changes markedly at different periods in the life
cycle, while the changes in the plumage show no sort of correspondence.
Charles Walker has noted that in young grackles the eyes are brown,
becoming lighter with age — the reverse of what happens in cats and
humans. In Brewer's blackbird {Euphagus cyanocephalus) the breeding
male has a pale yellow iris, the breeding female a light brown one. In the
rockhopper penguin, Eudyptes cristatus, the iris and the beak both vary
from yellow to red and back again with the seasons. One change is as
meaningless as the other, though both are doubtless expressions of the
ebb and flow of sex hormones in the blood stream.

Even more rapid color-changes of the eye may occur, presumably medi-
ated by dynamic changes in the iridocytes or perhaps by changes in the
optical properties of the iris stroma, induced in turn by changes in the
state of the iris muscles. Changes in the gross color of the iris have been
reported to occur, in emotional states and in illness, in cats and in an
occasional human. The eagle-owl of Europe, Bubo bubo, normally has
the usual strigine lemon-yellow iris; but when the bird is angry, accord-
ing to Arthur Thompson, the iris turns red and "seems to flash fire."

POSSIBLE VALUE OF EYE COLORATION 551

If the phenomenon is really as striking as all that, it may perhaps be
legitimately classed as a 'warning display'.

Fishes, despite their extensive dermal changes, show little or no
change in iris coloration with illumination. Trautman has noted, how-
ever, that in northern spotted bass (Micropterus p. punctulatus) dying
of anoxia, all dark coloration fades from the iris, leaving it red and
silvery. Ouradnik, while making color-photographs of narcotized rock
bass, accidentally found that the eye would turn red in response to elec-
tric shock. Apparently noxious stimuli may contract the melanophores of
fish irides, allowing other chromatophores to take charge of the color-
ation. But such phenomena cannot very well have any ecological signific-
ance.

Part 111 -Synoptic

Chapter 13
CYCLOSTOMES

(A) Lampreys

See also pages:
58 visual cells
117-8 embryology
126 Fig. 54c

127, 131 signif. of larval lens
128 primitiveness of ependyma
135-6,210 Fig. 60, taxonomic position,

habits, life-cycle
158 static pupil, lack of iris muscles,

nocturnal migrations
177 outer nuclear layer
184, 187 lack of area centralis
191, 199 yellow coloration of lens
193-6 value of yellow lens

251 Fig. 98

259-60 accommodation

264-5 optics

268 function of vitreous

272-3 Table VIII

291 visual field

338-9 median eyes

371 intra-ocular fluids

380 streamlining of eye

390-1 parasitic habits

406-7 macrophthalmia stage

449-52 spertacle

518-9 possibility of color vision

537-8 dermal color changes

Most lampreys live north of the equator, and these form the family
Petromyzonidse. In most of the genera of this family there are species
which are parasitic as adults. From each of these large lampreys, one
or more small, non-parasitic, 'brook' species has been derived. Some
slight simplification of the eye (but no true degeneration) has occurred
in all the brook lampreys, in keeping with the simplification of the whole
body and the life-cycle.

South of the equator live two genera of parasitic forms, Geotria and
Mordacia, which differ somewhat from each other and from the pet-
romyzonid lampreys. Each perhaps deserves family rank; but their re-
lationships are not yet sufficiently well known.

The Eye as a Whole — Of all non-degenerate vertebrate eyes, that of
the lamprey is the simplest. The ocular patterns of any two of the other
large groups of fishes will be found to differ from each other in only
one or two major characteristics. The lamprey eye lacks all of these
diagnostic features of higher fishes, and thus is primitive. But, it might
as easily add one feature as another : the lamprey eye is disappointingly
totipotential, and sheds no bright light upon the mode of origin of the
peculiarities of any 'higher' eyes.

555

556 CYCLOSTOMES

The lamprey orbit is not bounded, except in part, by the cranium,
but by a spherical connective-tissue capsule. The extra-ocular muscles
show some unique features, but none which could not — with a little
revision — be brought into line with the situation in other vertebrates.
They insert far forward, at the limbus, with some tendency to coalesce
there. The inferior oblique and the internal rectus originate together,
at a point farther nasally than the common point of origin (near the
optic nerve) of the other three recti. The inferior oblique and the in-
ternal and superior recti are supplied by the third cranial (oculomotor)
nerve, which in other vertebrates also innervates the inferior rectus (see
Fig. 70, p. 172), In lampreys however the sixth (abducens) nerve not
only supplies the external rectus as usual, but branches to the inferior
rectus as well. This nerve emerges from the brain unusually far forward,
and has been claimed to contain third-nerve fibers, which are perhaps
those which go to the inferior rectus. The superior oblique is identifiable
as such only by its nerve supply — from the fourth (trochlear) nerve —
for it has a unique location, and inserts on the ventro-temporal quadrant
of the eyeball. This has led some to refer to it as a 'posterior oblique',
and to suggest that it is not homologous with the superior oblique of
other vertebrate groups.

The corneal muscle (of accommodation), which is also outside the
eyeball, is homologous with the oculomotor muscles inasmuch as it de-
velops from one or two of the cephalic myotomes. It inserts into the
skin of the spectacle which covers the cornea (Fig. 161).

The eyeball, as in all groups of fishes, is flattened anteriorly so that
its antero-posterior axis is its shortest diameter. The major (equatorial)
diameter varies from about 1.5mm. in the smallest brook forms {e.g.,
Ichthyomyzon fossor, Eudontomyzon cepypterus) to about 6.0mm. in
the larger parasitic petromyzonids {e.g., Entosphenus tridentatus, land-
locked Petromyzon marinus) and 7.0 mm. in Geotria australis.

The virtual space between the dermal spectacle and the cornea is
occupied by a delicate mucoid tissue (thick in brook lampreys, thin in
larger forms, where it may be almost lacking under the center of the
spectacle), which belongs to neither structure, but is rather a continu-
uation of the lining of the orbital capsule. The sclera is a thin membrane
in, brook lampreys. In the larger parasitic species it is relatively and
absolutely thicker, and in the fundus may be as thick as the retina; but
it is always purely fibrous in structure, never with any embedded carti-
lage or bone. Such a sclera may of course descend from an ancestral

THE LAMPREY EYE

557

cartilaginous one, as have those of the placental mammals and the
snakes. Here in the lampreys however it may be regarded as primitive —
particularly if one adheres to the dural theory of the evolutionary origin
of the sclera (see p. 119), rather than to the older idea of a cartilag-
inous 'optic capsule' accompanying the hypothetical original chondro-
cranium. The cornea is very thin in all lampreys, consisting of little more
than a Descemet's mesothelium and a thick Descemet's membrane.
Since the cornea and the skin have not fused, there is of course no
corneal epithelium — contributed in higher forms by the epidermis of
the skin.

Fig. 161 — The eye and surrounding structures in a lamprey, Lampetra fluriatilis, in
horizontal section; the anterior end of the animal is to the left. Modified from Franz.

av- anterior surface of vitreous; er- external rectus; to- inferior oblique; ir- internal rectus;
n- optic nerve; s- speaacle; sk- skin; sp- subsjiectacular space (virtual, and occupied by a
mucoid continuation of the orbital capsule); sr- superior rectus; /- tendon of corneal muscle,
inserted in spectacle; v, v- venous sinuses.

In the European river lamprey, Lampetra fluviatilis, the inner surface
of the cornea, near the iris angle, bears a conspicuous thickening com-
posed of epithelioid cells, much like the annular ligament of a teleost
(see Fig. 169, p. "y??) . The cells may represent a piling-up of Descemet's
mesothelium, though it has been claimed that the mesothelium passes
over them and reflects onto the anterior face of the iris. The writer can
see nothing of such an arrangement. No function has been suggested for
the thickening. Delicate strands, perhaps coated with mesothelium, cross
from it to the periphery of the iris, like a pectinate ligament. These

558 CYCLOSTOMES

Strands are present even in brook lampreys, in most of which the thick-
ening is practically non-existent (except superiorly), and also in other
parasitic lampreys — none of which has it so prominent as Lampetra.

The chorioid appears to differ markedly between parasitic lampreys
and the various brook species in the same genera with them. In Lampetra
fluviatilis and Petromyzon marinus, perhaps also in Entosphenus trident-
dtus (where an especially intense pigmentation interferes with obser-
vation), the outer half or more of the thick chorioid consists of a con-
tinuous lake of blood, the 'subscleral sinus'. This is presumably fed
directly by the choriocapillaris, which in turn is supplied by small arteries
in the more ordinary, inner, portion of the chorioid. The chorioid has no
true veins; the arteries branch away from four main ones, one in each
quadrant, which stem from a single artery which perforates the sclera
just beneath the optic nerve. The chorioidal sinus is drained through the
sclera by four apertures, called Venae vorticosae' by courtesy, into a
system of extra-ocular venous sinuses (Fig. 161, v, v) which fill the
orbital capsule and cushion the eyeball, much as does the orbital fat of
a higher vertebrate. These sinuses are present in brook lampreys also;
but here, the chorioid is usually no thicker than the pigment epithelium
of the retina, and indications of a subscleral sinus can be seen fairly
clearly only in such large species as Entosphenus lamottenii (= appendix).

The iris has smooth inner and outer surfaces. The posterior layer of
its retinal portion contains pigment only in the parasitic species, and
then but little, mostly concentrated near the pupil. The anterior layer,
which in other vertebrates gives rise to the sphincter and dilatator pupil-
lae, is epithelial and heavily pigmented in all lampreys. This situation is
quite diagrammatically primitive, for the iridic continuations of the
retinal pigment epithelium and the sensory retina thus preserve their
respectively pigmented and unpigmented conditions in lampreys, instead
of exchanging them (contrast Fig. 7g, p. 15). The lamprey iris possesses
but little stroma, this in turn with little pigment or none. In brook forms,
there is just enough stromal tissue to hold together the thin layer of
blood vessels, which lies immediately against the retinal layers and forms
apparently the anteriormost tissue of the thin iris. Large lampreys how-
ever have a substantially thick argentea layer anterior to the blood-vessel
layer. It does not continue around the chorioid (c/. pp. 235-6). The
blood-vessel layer in all lampreys is much like a choriocapillaris; but it is
independently fed by three small, symmetrically-arranged arteries which
enter the eyeball anteriorly.

THE LAMPREY EYE

559

The iris merges directly into the chorioid opposite the ora terminalis
of the retina, without the intermediation of a ciUary body — since there
are no ciUary muscles, ciliary processes, or zonule fibers, for which attach-
ments need be supplied. The perfectly spherical lens is held against the

a ^XaragnJ

Fig. 162 — Retina and optic nerve of Lampetra fluviatilis.

a, appearance in ordinary histological preparation, x 500.

a- amacrine cells; b- bipolar nucleus; c- cone; g- ganglion cells; h, h- horizontal cells;
m- Miiller fiber; n- nerve-fiber layer; o- outer nuclear layer; p- pigment epithelium; r- rods;

b, neurological schema, based upon Bielschowsky preparations, x 250. After Tretjakoff.

a, a- amacrine cells (six types); b,b- bipolar cells (five types); c- cone; e- external limit-
ing membrane; g- ganglion cell; h- horizontal cells; i- internal limiting membrane; m-
Miiller fiber; n- nerve-fiber layer (= ganglion-cell axons); r- rod.

c, cross-seaion of optic nerve and its sheaths. From Franz, after Diicker.

d- dural sheath; pa- pia-arachnoid sheath; n- nerve-fiber mass; e- ependymal cell-bodies;
oa- ophthalmic artery.

560 CYCLOSTOMES

cornea by the vitreous. The surface ('hyaloid') membrane of the latter
is conspicuous in microscopic sections, but it contains no blood vessels
where it contacts the retina. Indeed, apart from the iris and chorioid
there are no vascularized structures; and there is no canal of Schlemm.

The Retina — The lamprey retina (Fig. 162) differs from all others in
that its ganglion cells are not separated from the inner nuclear layer.
As a consequence, the nerve fiber layer lies embedded high in the retina
instead of near its inner surface (cf. Fig. 19, p. 43). Though one cannot
be certain, it is not likely that this is a primitive arrangement (nor does
it smack of 'degeneracy') . True, in the histogenesis of any (other) retina
the bodies of the ganglion cells are at first contiguous with those of the
inner-nuclear elements; but it is stretching a point to suggest that this
is an ontogenetic recapitulation of the adult cyclostome arrangement.

The lamprey optic nerve is, however, assuredly primitive in its organ-
ization. Running axially through it is a column of cell-bodies, appearing
in cross-sections of the nerve as a rosette of nuclei, each of whose single
processes radiates to the surface of the nerve. These cells are obviously
ependymal — not of a higher, glial, type (which they have usually been
called). If we think of the optic nerve as a cylinder, then its radius
represents morphologically the thickness of the neural tube of which the
retina is an evagination. The axis of the nerve — even though the nerve
is not tubular, but solid — thus stands for the inner surface of the brain
wall. Thus, each ependymal cell in the optic nerve maintains the orien-
tation of any ependymal cell in a primitive brain (see pp. 126-9). Verte-
brates above the lampreys all have at least neuroglial tissue, if not meso-
dermal connective tissue as well, forming the supporting framework of
their optic nerves.

The visual cells of lampreys exhibit variations from genus to genus,
but within the Petromyzonidse these can be arranged in a fairly satis-
factory series with regard to taxonomy. In the primitive genus Ichthy-
omyzon the rod and cone differ but little in length, and the outer seg-
ments of both are tapered, and to this extent, 'cone-like'. The rods out-
number the cones by five-to-one in the parasitic lake species castaneiis
and unkuspis, by three-to-two in the brook form fossor. In Petromyzon
(Fig. 163b), the next higher genus in the scale, the cones have become
much longer than the rods; and the rods, which here outnumber the
cones three-to-one, have cylindrical outer segments of moderate length.
This differentiation in length and shape reaches a maximum in Ento-
sphenus, and the numerical predominance of the rods is greatest also in

THE LAMPREY RETINA

561

E. tridentatus (8:1; in lamottenii, 1 :1). Lampetra fluviatilis (Fig. 162),
though a member of the culminant genus of the petromyzonid line, has
its rod and cone outer segments of less unequal length, and even the rod
outer segments are slightly tapered — thus, rod and cone are rather less
well differentiated than those of Entosphenus, ranking just below Lam-
petra. The 1 : 1 ratio of rods to cones in fluviatilis — so close to the ratios
in all brook lampreys, regardless of their taxonomic affinities — probably
reflects the shallow-water habitat. The rods outnumber the cones most

a b

Fig. 163 — Visual cells of lampreys and elasmobranchs. x 1000.

a, 'cone' types (at least one of them functionally a rod) of New ZealanH lamprey, Geotria
australis.

b, cone and rod of landlocked Atlantic lamprey, Petromyzon marinus.

c, cone and rod of smooth dogfish, Mustelus cants (redrawn from Schaper). In M. mustelus
the cone is less rod-like in form, and in Myliobatis aquila it is fully differentiated; all other
elasmobranchs have only rods, like that shown here.

greatly in the lake and marine lampreys, which, for their life in deeper
waters, might be expected to require more rods for greater sensitivity
to light.

On morphological grounds alone, it appears probable that the pet-
romyzonid rod has evolved from a cone within the group, with Ichthyo-
myzon exhibiting an early stage in the process; and, from taxonomic
considerations, it would seem that this rod must then have no connection
with any other in the vertebrates (see Plate I). The visual cells of

562 CYCLOSTOMES

Geotria (which genus some ichthyologists consider more primitive than,
perhaps ancestral to, the petromyzonids) are all cone-like in form, and
comprise three types in about equal numbers. The largest of these types
may however contain rhodopsin as does the short (rod) cell in the
petromyzonids — unlike the northern lampreys, Geotria is nocturnal, and
should have at least one type of functional rod. In any event, the average
petromyzonid pattern (Fig. 163b) shows neither an easy derivability
from that of Geotria (Fig. 163a) nor any ready convertibiUty into the
pattern of duplex selachians (Fig. 163c).

No well-preserved material of Mordacia has ever been described. As
nearly as Franz could make out in his sections, most of the visual cells
are identical and are rod-like in form, with interesting 'false oil-droplets'.
The retina may truly be pure-rod, for the tiny pupil (0.2mm, in diam-
eter in a 3.0mm. eyeball) suggests a sensitive retina. In that case, it was
probably derived from an ancestral pure-cone one, something like that
which Geotria appears to have, by transmutation (see Plate I).

(B) Hags

In the hagfishes the eye may be nearly as large as that of a small
species of brook lamprey; but it is quite degenerate, and these animals
give no response to light. In Eptatretus and Polistotrema the eyeball,
1.0mm. (E. dombey) to 1.3mm. (P. stouti) in diameter, lies embedded
at the skinward side of a mass of fat three times its size, which in turn
is situated at a variable distance beneath the skin. There are no extra-
or intra-ocular muscles, no nerves except a vestigial optic, and there is
no pigment in either retina or uvea. There is no trace of a lens, though
in the embryo a lens placode forms and then thins out as if discouraged.
The sclera and chorioid are not differentiated from each other (c/. the
normal embryology of these tissue's — pp. 114-6); and the adult retina,
only half as thick (lOO[x) as the average vertebrate retina, is still actually
an optic cup with a considerable remnant of the old optic-vesicle cavity
(see Fig. 38, p. 106). In some individuals, the embryonic fissure persists.

The eye of Myxine glutinosa is even more completely degenerate
(Fig. 133a, p. 387). The half-millimeter eyeball is practically filled by
the retina, which is doubled so sharply upon itself that there is no room
for a vitreous cavity.

Chapter 14

HIGHER FISHES

(A) Elasmobranchs

See also pages:

1 18 optic vesicle

135-6 Fig. 60, taxonomy, anatomy

150 photomechanical changes

155 lids

157-9,219-22,224,256 pupils

184-7, 243, 245 area centralis

200 habits

216 visual cells

225 Fig. 91

240, 243-5 tapetum lucidum

251, 260, 272-3, Fig. 99, accommodation

255 ramp retina in rays

262 protraaor lentis, ciliary folds

264 optics

265 persistent embryonic fissure
266-7 comparison with amphibians
372 zonule
comparison with snakes
hammerhead visual field

268,
282
291
303
338
372
380

eye movements

median eyes

water-balance

ellipsoidality of eyeball
384-6 adaptation to the bottom
392, 394, 397-8, 402 deep-sea spp.
415-6 thickness of sclera
428-9 lids, other peculiarities
518-9 possibility of color vision
537 dermal color changes

Most families of sharks and rays are tropical or subtropical, with
pelagic or benthic habits. The permanent residents of the temperate
zones are mostly bottom-living forms. A few species of both sharks and
rays live in fresh water. The chimeras are all deep-sea, bottom fishes.
The ocular specializations of elasmobranchs are in the direction of dim-
light activity, and most species are nocturnal.

The Eye as a Whole — Elasmobranch eyes are large relative to the
body — largest of all (and with the largest lenses in proportion) in the
chimxras and such deep-sea sharks as Etmopterus, relatively small in
the partly-skyward-looking rays, smallest of all (except for an enormously
overgrown scleral cartilage) in such blind deep-sea rays as Benthobatis.
Mobile upper and lower lids, sometimes also a nasoventral 'nictitans',
are usually developed to a greater or lesser degree in sharks (Galeorhin-
idae, especially), though without any obvious value to the animal (see
Fig. 131b, p. 382). In forms whose nictitans is very active, the lower lid
(of which the nictitans is really a continuation) is motionless. The nicti-
tans alone is present, together with a circular, motionless lid-fold, in the
hammerheads (genus Sphyrna, —^ygcena).

563

564

HIGHER FISHES

The oculomotor muscles of adults are orthodox, though in the embryo
(in Squalus, at least) a mysterious extra muscle ('muscle E') appears
and then degenerates. In Chimcera, which is primitive in many anatom-
ical respects, the internal rectus originates far nasally as in lampreys;
but in most elasmobranchs the four recti originate close together, and
the orbit ordinarily affords room for them to form a cone as in mammals.
They insert at about the equator of the eyeball, the internal rectus how-
ever a little behind and the external a bit ahead. The obliques originate
close together, far forward, and share insertion-sites with the correspond-
ing vertical recti. This arrangement — probably more primitive than that
in living cyclostomes — is essentially preserved in higher fishes, and

Fig. 164 — The eye of a shark, Carchawdon carcharius. xWi.
Combined from figures of Franz.

a, horizontal, b, vertical seaion. c- cornea; c/- ciliary folds, forming anchorage of gelatin-
ous zonule; ch- chorioid; ext- external rectus; «'- iris; inj- inferior reaus; int- internal rectus;
/- lens; op- optic pedicel; p- lens-muscle papilla (c/. Fig. 166); r- retina; s- suspensorium of
lens; /c- scleral cartilage; t/- fibrous portion of sclera; lo- superior oblique; /Mp- superior rectus.

indicates that the original function of the obliques was to impart
compensatory reflex wheel-movements to the eyeball in the plane
of its equator (Fig. 163; cj. Fig. 16, p. 37, and p. 303).

A characteristic structure of the orbit is the cartilaginous optic pedicel,
running prop-like from cranium to eyeball. At the eyeball end, it is often
expanded and cupped to fit a broad, low boss on the back of the sclera,
thus forming a ball-and-socket joint for the rotation of the eyeball. In
various genera it may be lacking (Scylliorhinus, deep-sea forms; always
through disappearance?), or may not reach to the eyeball, or may even
contact the eye but not the cranium (Sphyrna) . In a few forms — sharks
as well as rays — it is slender and so bent and elastic that its tendency to
straighten itself can proptose the eyeball when the extra-ocular muscles

THE ELASMOBRANCH EYE

565

relax all together. This action, having the effect of a levator bulbi muscle,
was perhaps its ancient, original function. Apart from the pedicel, the
eyeball in various elasmobranchs is supported and cushioned in the orbit
by masses of gelatinous connective tissue, lymph- or blood-sinuses (cf.
lampreys) , or combinations of these.

In sharks and chimaeras the eyeball is regular in shape and usually is
strongly ellipsoidal, with its longest diameter horizontal and its shortest

Fig. 165 — Hypothetical primitive arrangement of
the extra-ocular muscles in gnathostome fishes.

(The diagram shows the eyeball and the muscles as
seen from the dorsal side, and emphasizes the favor-
able orientation of the obliques for the production
of simple wheel movements of the eyeball in the
plane of its equator).

ext- external rectus; inf- inferior rectus (revealed
through gap in superior rectus ) ; int- internal rectus;
io- inferior oblique (revealed through gap in supe-
rior oblique); n- optic nerve; so- superior oblique;
sup- superior rectus.

Fig. 166 — Anterior segment of

Mustelus mustelus. x5. Combined

from figures of Franz.

/- lens; Im- lens muscle (black);
p- lens-muscle papilla; r- retina;
s- suspensorium of lens; sc- scleral
cartilage.

diameter the antero-posterior axis (Fig. 164). The eye is quite homog-
eneous structurally in these forms, with its greatest variations occurring
in the sclera, which may be very thin as in chimaeras and some deep-sea
sharks {e.g., Etmopterus) , or extremely thick as in the largest sharks.
In one deep-sea shark, Lcemargus, perhaps as a mark of degeneracy, the
sclera sends massive cartilaginous diverticula into the chorioid. In most
rays the depression of the body has involved the eyeball, producing a

566 HIGHER FISHES

distortion which may be best described as a flattening of the anterior
dorsal region (Fig. 102b, p. 255).

The sclera is thickened not only fundally, to receive the optic pedicel,
but also at the muscle-insertions and in a zone surrounding the cornea.
It is usually thinnest at the equator. The sclera consists largely of a cup
of hyaline cartilage, which is often calcified. The cornea is thick peripher-
ally (and often opaque there, particularly dorsally and ventrally), thin-
ner centrally, and is strongly arched in contrast to the flat comeae of
other kinds of fishes. The cornea is claimed to have all of the layers
characteristic of the human, and even has a thick Bowman's membrane ;
but while a very thin, hard-looking cuticular membrane similar to a
Descemet's membrane is present on the inner surface, the writer can
make out no mesothelium whatever lying upon it iSqualus acanthias) .
The substantia propria is very neatly laminated, the fibers of each layer
becoming progressively thinner toward the center of the cornea. Much
of the thinning of the corneal center is accomplished by a dropping-out
of layers, however. The epithelium may possess several times as many
layers of cells as the human; but it is not cornified.

The chorioid is heavily pigmented, and typical in structure except for
the inner one-fifth or so of its thickness, which in nearly all species is
modified to form the remarkable tapetum lucidum characteristic of the
group. Over a restricted area in the fundus, the chorioid is often mark-
edly thickened by the presence, on its scleral side, of a so-called 'supra-
chorioidea'. This may consist of connective tissue with some blood-supply
from large veins embedded in it, or it may consist largely of a tangle of
such veins (possibly, then, a modification of the cyclostome subscleral
sinus) . The suprachorioidea is lacking in those species in which the optic
pedicel is absent or is incomplete in extent, and the same reason seems
to cover both lacks : less room than usual in the orbit, owing to a par-
ticularly large eyeball. To accommodate a suprachorioidea, the sclera is
bowed outward, and the curvature of the retina is thus not disturbed.
Between suprachorioidea and sclera there are believed to be lymph
spaces, so that the chorioid and sclera are not conjoined firmly except
near the limbus. Two arteries enter the eyeball, one temporally (which
supplies the chorioid), the other ventrally (which runs forward through
the chorioid to supply the iris) ; and two main veins, one dorsal, one
ventral, leave it. Only the uvea is vascularized in the adult, though in
embryos a vessel has been found to enter the embryonic fissure about
midway of its length, thence sending branches forward and backward

THE ELASMOBRANCH EYE 567

along the retinal surface. This vessel is squeezed inexorably forward
during development, however, as the embryonic fissure heals itself pro-
gressively forward from the fundus toward the periphery of the optic
cup. The adult counterpart of this vessel may be the tiny one which
supplies the lens-muscle papilla (v./.).

The thin, broad, amuscular ciliary body bears low folds anteriorly,
which may run up onto the back of the iris, and always leave a smooth
orbicular zone behind them, toward the ora terminalis. The folds are
meridional in sharks, but in rays are restricted to the dorsal and ventral
quadrants (like the ciliary folds of the few teleosts that have them; and
like the iris folds in many amphibians). A gelatinous zonule, shaped
like a washer with a thickened rim, is anchored to the coronal region
and to the lens near its equator. Further support is given the lens by a
median dorsal, downward extension of the ciliary body into the zonule,
forming a 'suspensory ligament'. Ventrally, the lens rests upon a cushion-
like protuberance of the ciliary body. This papilla is in turn supported
erect by a fin-like continuation of itself onto the back face of the iris.
It is along the crest of this fin that the protractor lentis, the muscle of
accommodation, is placed (Fig. 166). This little muscle is a derivative
of (and indeed remains intercalated in) the pars ciliaris retinae covering
the papilla; hence, it is ectodermal. In its gross anatomical relationships,
the lens-muscle papilla varies considerably from genus to genus of elas-
mobranchs; and as an extreme of this variation it may give a fair
imitation of a teleostean falciform process together with its campanula
(^.v., pp. 582-3) — with which some of the elder anatomists seem to have
confused it.

The iris is bowed forward in its middle by the subspherical lens, mak-
ing the anterior chamber extremely shallow. Histologically, the iris is
much like that of the parasitic lampreys, but with considerable pigmented
stroma underlying the argentea (which, as in lampreys, is confined to
the iris and does not embrace the chorioid) . Some blood vessels are free
in the stroma, but most lie against the retinal layers at the back of the
iris. The posteriormost of the two retinal layers is devoid of pigment
toward the root of the iris (as also in the ciliary body, as usual), but
takes on more and more pigment toward the pupil until, for the pupil-
lary one-third or so of the radial width of the iris, both retinal layers
are heavily and about equally pigmented. The epithelio-muscular ele-
ments of the sphincter and dilatator (the former not so well separated
from the parent epithelium as in man) are spindle-shaped, pigmented.

568 HIGHER FISHES

and autonomous and sluggish in their action. This musculature is scant
in the deep-sea elasmobranchs, whose wide pupils are almost permanently
open. At the root of the iris, the organ makes a slender angle with the
cornea. There are no pectinate or annular ligaments in the iris-angle
region, no loose meshwork tissue, and there is no canal of Schlemm.

The Retina — The elasmobranch retina is characteristically pure-rod,
with a high ratio of visual to ganglion cells. This great summation helps
to confer the photic sensitivity upon which the light-shunning habits of
these fishes are based; but it necessitates a low visual acuity — estimated
by Franz to be, on the average, 5% of that of man. Franz determined
the number of fundal rods to be 10,800/sq. mm. in Raja batis, 21,600 in
Torpedo, 24,000 - 75,000 in various small sharks, 100,000 in Chimara,
and 132,000 in Etmopterus. Corresponding ganglion-cell estimates were :
Ra]a batis, 1500; Torpedo, 5000; the small sharks, 1200 - 3600; Chi-
mcera, 600; and Etmopterus, 900.

The pigment epithelium is devoid of pigment (and usually, of cell-
processes) over the whole extent of the sensory retina in all elasmo-
branchs except those few which lack the tapetum lucidum for obvious
reasons : Lcemargus (an abyssal shark) , Selache (the basking shark) , and
Myliobatis (a pelagic ray with a cone-rich retina).

The horizontal cells in elasmobranchs are massive, much like those
of lampreys (see Fig. 162a, b; p. 559). Though fine processes have been
seen on them in Golgi preparations, it is unlikely that they have any-
thing but a supporting function. The bipolar, amacrine, and ganglion
cells are not confined to their 'proper' nuclear layers, but may occur out
of position, in layers above or below. Such misplacements are quite char-
acteristic of crude, scotopically-adapted retinas in lower vertebrates.

Cones are known to occur only in one dogfish genus iMustelus), the
eagle ray Myliobatis aquila, and (doubtful!) the monk-fish, Squatina.
They are least distinct from the rods, morphologically, in Mustelus
canis (Fig. 163c, p. 561), better differentiated in M. mustelus, and are
completely cone-like {i.e., short, with plump inner segments and small
outer ones) in Myliobatis, according to Mile. Verrier. It seems clear
that these few modern-elasmobranch cones are 'new', secondary deriv-
atives of rods; but, the 'original' vertebrate cone must have persisted
through the ancient elasmobranchs, in order to be handed on to the
higher fishes — none of which, of course, were derived from sharks, rays,
or chimaeras (see Plate I).

ELASMOBRANCH RETINA; CHONDROSTEAN EYE 569

The optic nerve has various cross-sectional shapes and septal patterns
in the various species. In some, an axial core of ependymal or glial cell-
bodies persists in the adult, reminiscent of the situation in the lampreys
(p. 560; see Fig. 162c, p. 559).

(B) Chondrosteans

See also pages: 235-6 argentea

135-7 Fig. 60, taxonomy 238-42 Fig. 96, tapetum lucidum

150 photomechanical changes 264, 272-3 accommodation

160, 220-2 pupil 292 binocular

vision

174 eye size and shape, optics 381 streamlining

187 lack of area centralis 415-6 sclera

200-2 oil-droplets 519-20 color vision

The living Chondrostei include the twenty-odd species of sturgeons
(and shovel-nosed sturgeons) and the two genera of spoonbills, Poly-
odon and. Psephurus. Most sturgeons are marine and anadromus; but
a few (and the spoonbills) are confined to fresh water. All are bottom-
feeders, with scotopically-adapted eyes. The eyes of the spoonbills have
had practically no attention, and the ensuing statements apply solely
to the sturgeons.

The Eye as a Whole — The firm margin of the orbit forms a broad
horizontal ellipse, and is supported dorsally and ventrally, in the com-
mon European sturgeon (Acipenser sturio) and some others (but not
A. nasus) by a pair of crescentic bones embedded in the conjunctiva.
These have no phylogenetic connection with the scleral ossicles of either
teleosts or sauropsidans. There are two venous sinuses in the orbit in
most species, but the really important 'packing' around the eyeball con-
sists of connective tissue. Concerning the extra-ocular muscles, no peculi-
arities are on record. The eyeball and cornea are slightly oblong hor-
izontally, but not as much so as in most sharks.

The sclera is again cartilaginous, as in the elasmobranchs (and indeed
all vertebrates excepting the cyclostomes, some teleosts and urodeles, the
snakes, and the non-monotreme mammals). Obeying the 'rule' that
where a relatively small eye lies in a large body its sclera is dispropor-
tionately thick (see p. 415), the scleral cartilage in the largest stur-
geons is monstrously thickened in close imitation of the largest sharks
(Selache, Rhineodon) and the whales (Fig. 167; cj. Fig. 141a, p. 413).
It is of reasonable thickness, however, in such small-bodied, relatively
large-eyed species as the American rock sturgeon, A. fuhescens. The

570

HIGHER FISHES

cornea is somewhat thinner centrally than peripherally, and is cloudy
at its dorsal and ventral margins, as in elasmobranchs. In contrast to the
latter, the sturgeons have a prominent Descemet's mesothelium, which
is piled up at the iris angle to form an annular thickening from which
a loose meshwork bridges over to the iris, isolating a large space com-
parable to that of Fontana in mammals (see pp. 679-80) .

The chorioid is about as thick as the retina (and only a quarter as
thick as the sclera), except for a small area in the fundus where a
suprachorioidea of richly vascular character (as in some elasmobranchs)
is superimposed upon it externally. To receive this, the sclera is locally

Fig. 167 — Eye of a large sturgeon, Acipenser sturio. xlVi.
From Franz, after Soemmerring. co- conjunctiva; sc- scleral
cartilage; ct- connective tissue; on- optic nerve.

Fig. 168
Cone and rod from retina
of a sturgeon, Acipenser
fulvescens. xlOOO.

thinned, not evaginated. The chorioid is silver-plated inside and out.
The inner two-fifths of its thickness is occupied by the laminated, cellular,
guanin-laden tapetum lucidum (Fig. 96, p. 242), which is separated from
the retinal pigment epithelium only by the choriocapillaris, and extends
forward even beyond the ora terminalis to dwindle away opposite the rim
of the scleral cartilage. Externally, the chorioid is covered by a (thinner)
layer of guaninized tissue — a true argentea, exactly comparable with
that of Amia and the teleosts (and presumably directly ancestral there-
to) . It is as if either the tapetum or the argentea had been evolved first
in the sturgeons, and the other of the two created by delamination, with

THE CHONDROSTEAN EYE 571

the unmodified chorioidal layers somehow getting in between them. In
all probability, however, the sturgeons' argentea and tapetum were quite
separate inventions despite their superficial histological resemblance. The
argentea clings to the sclera even over the bump formed on the chorioid
by the suprachorioidal cushion, and extends into the iris. Here it splits
up into many lamellse which occupy the whole thickness of the iris stroma
and are sandwiched between layers of stromal connective tissue. The
vascular supply of the eyeball, which relates solely to the uvea, has not
been well worked out; but it apparently resembles somewhat the arrange-
ment in elasmobranchs.

A 'ciliary body' can be recognized, with a little effort, between the
ora terminalis and the portion of the uvea which is unmistakably freed
from the fibrous tunic to form the iris ; but its uveal portion is amuscular
and differs in no important histological respects from the chorioid proper.
In some European forms, this narrow zone is said to have meridional
folds; but in A. julvescens it is smooth. In all species, however, there is
a mid-ventral papilla whose structure and homologies remain to be fully
elucidated. Though it has been compared both with the elasmobranch
lens-muscle papilla and with the teleostean campanula, it is not actually
known to develop, embryologically, after the fashion of either. It appar-
ently contains no muscle fibers, for Hess was unable to elicit any accom-
modatory changes in sturgeon eyes under electrical stimulation. The
slightly flattened lens (Fig. 167) is suspended by a ligament quite like
that in teleosts (see Fig. 105g, p. 261; Fig. 169, p. '^77).

The iris is devoid of muscles, so that if we imagine the sturgeon eye
to have evolved rather directly from one like that of a modern shark,
we must say that it has reverted to the muscle-free condition of the lam-
preys— owing to the adoption of the bottom habit, with a renunciation
of any shark-like tendency to bask (which would call for a mobile pupil
to protect the sensitive retina developed for the benthic mode of life) ;
and with a discard of accommodation, this being of no value to a
scotopic eye with its crude resolution. In different quadrants* the pig-
mentation and the argenteal content of the iris stroma vary reciprocally,
as if either reflection by the argentea or absorption in pigment were
alone adequate to prevent light from getting through the tissue. But in
regions where the iridic argentea is conspicuous, the distribution of

* Unfortunately the writer cannot be more specific, for the plane of section of his material
{A. fulvescens, prepared by the late Harold D. Judd) is uncertain.

572 HIGHER FISHES

fuscin pigment in the retinal layers is as in elasmobranchs (p. 567) ;
whereas, where there is much stromal pigment and little or no guanin,
the posteriormost epithelial layer of the iris is quite unpigmented, as
in lampreys.

The Retina — The sturgeon retina is characterized by a peculiar pig-
ment epithelium, normal enough in its heavy pigmentation where it
covers the 'ciliary body', but modified opposite the entire sensory retina
in a manner best understood in connection with the discussion of the
tapetum — pp. 238-9. Another peculiarity is the virtual absence of any
distinct inner nuclear layer. The neuron cell-bodies which should form
such a layer are displaced upward or downward by the great mass of
horizontal cells (Fig. 96, p. 242) ; and the Miiller fibers are not evenly
distributed, but gathered into great bunches, their nuclei squeezed up to
the lower surface of the outer nuclear layer. The outer nuclear layer is
essentially single, but ragged, with the cone nuclei lying above the ex-
ternal limiting membrane, and the rod nuclei nearly always below it
except in the periphery. Summation in the scanty ganglion cells is very
great, and the overall threshold of stimulation of the retina should be
very low, in keeping with the habits of these fishes.

The visual cells (Fig. 168, p. 570) are of two types — large rods, and
single cones in smaller number. Here, for the first time (phylogenetic-
ally), we encounter cone oil-droplets in an extant vertebrate group. The
oil-droplets are completely colorless in life (A. fulvescens, at least), but
were assuredly not always so. The very fact that so many cones are
present — though with their oil-droplets bleached in sympathy with a
present avoidance of strong light — together with the presence of an
apparently vestigial mechanism for moving the lens (the papilla de-
scribed above, which suggests that the ancient chondrosteans did have
accommodation), indicates that the primitive chondrosteans were diur-
nal, probably with smaller rods, more cones, and an accommodation
equal to that of the teleosts. Moreover, though double cones (which are
associated with bright-light vision) are lacking in living sturgeons, their
presence (and identity of plan) in both the holosteans and the amphib-
ians shows that the common ancestors of these groups, the primitive
Chondrostei, must have had them (and presumably invented them; see
Plate I) . The oil-droplet is probably even more ancient, and indeed may
have been present in the visual cells of vertebrates before these were
visual in function : such pigmented oil-droplets are common in pigment-

CHONDROSTEAN RETINA; HOLOSTEAN, TELEOST EYES

573

epithelial cells (which are of course homologous with rods and cones) ;
and similar vacuoles occur in some {Atnby stoma) ependymal cells (see
pp. 126-9 and Plate I).

(C) HOLOSTEANS AND TeLEOSTS

See also pages:

5 visual consciousness

44 Fig. 20e

52 optic chiasma

54 Fig. 22b

55 Fig. 23c

57-8, 60-1, 175-6, 216-7 visual cells

59 Fig. 24e

118 embryology

127 Fig. 55d

131 origin of lens muscle

134-5, 137 Fig. 60, taxonomy

145 habits

146-53 photomechanical changes

154, 157, 219-222, 228, 257 pupil

157,231,373-5 rhodopsin

158 Fig. 65

160-1 pupil, iris muscles, optics

164 energy economy

174 eye size and shape, optics

179 blind spot, optic nerve

184-5, 187, 190, 303-5 Fig. 77b, area and

fovea
191, 193-6, 200-2 yellow cornea and its

value

204, 405-7 eels

210, 212-3, 384-405 bottom, cave, para-
sitic, deep-sea fishes

230-241 eyeshine, tapetum

235-6 argentea

251, 254, 257, 260-3, 272-3 Fig. 98,
accommodation

264-5 optics

268 value of vitreous

271, 380-1 Fig. 130, scleral ossicles

277 ciliary muscle

289-93, 320, 323-5, 331, 376-9 visual
angles and fields

300-5 eye movements

349 movement-perception

362-5 stroboscopic vision

364, 466-7, 472-90, 518-9, 521-2 color
vision

369-76 ocular adaptations to water

379-80 streamlining

381-4, 418 lids

414 comparison with whales

431-6 amphibious vision

450-4, 459-61 spectacles

524-37 dermal color changes

543-51 coloration of eye

The only living holosteans are the bowfin or freshwater dogfish (Amia
caha) and the several species of gars (genus Lepisosteus). All are con-
fined to North American fresh waters. Amia is restricted to the United
States; Lepisosteus reaches south to Panama. Ancient holosteans were
the ancestors of the teleosts, which are cosmopolitan and greatly out-
number all other kinds of fishes put together. The eyes of the handful
of holosteans are best treated here together with those of the 20,000
species of teleosts; for, to all intents and purposes, the holostean eye
is a teleost eye.

Holosteans — The extra-ocular muscles are normal in adults; certain
of them run through canals in the bones of the skull. In Amia larvae,

574 HIGHER FISHES

the internal rectus has a more anterior origin (primitive? — cf. lampreys,
Chimcera) , migrating backward during growth. The eyeball is somewhat
ellipsoidal in Lepisosteus {e.g., 19.5mm. horiz. X 17.5mm. vert. X 15.0
mm, axial), but is spherical in Amia.

The scleral cartilage is hyaline and thick, but is thinned fundally in
Amia where it surrounds the 'chorioid gland' (v.i.). The cornea is like-
wise thick, as in large-eyed teleosts. The fibrous substantia propria is
homogeneous; there is no canal of Schlemm. Descemet's mesothelium
thickens at the iris angle to form a massive annular ligament, a cushion
of epithelioid cells (said to contain glycogen) applied to the cornea.
This thins abruptly to reflect onto the anterior surface of the iris, which
thus has a mesothelial facing extending nearly to the pupil margin. Amia
is the lowest vertebrate for which the presence of such a layer on the
iris can be asserted with any assurance — and it is by no means certainly
present in all forms above the holosteans.

The chorioid of Amia (but not of Lepisosteus) is modified by the
presence of a chorioid gland. This structure, which is highly character-
istic of the teleosts, is not a gland but rather is a great mass of capillaries,
a three-dimensional rete mirabile. Its function is unknown, but it is prob-
ably not primarily nutritive. The best guess so far made is that it serves
to smooth out the fluctuations of intra-ocular blood pressure which the
heart-beat tends to produce, and thus insures a smooth flow of blood in
the chorioidal vessels supplied from it, freeing the retina from mechan-
ical disturbance. In Amia, as in teleosts, it is shaped like a bloated horse-
shoe, straddling the optic nerve with its opening directed ventrally. It is
larger in Amia than in any known teleost, and is responsible for the
spherical shape of the eyeball of Amia — whose actual intra-ocular cavity
is flattened antero-posteriorly as in fishes generally.

There is an argentea, present only ventro-temporally in Lepisosteus
but complete in Amia, where it splits into two layers to enclose the
chorioid gland. The innermost of these layers comes almost close enough
to the back of the retina to serve as a tapetum (like that in sturgeons)
if it were wanted — but since most of the pigment in the chorioid is con-
centrated in a thin layer just outside the choriocapillaris, the inner ar-
genteal layer is hors de combat as a reflecting device. Besides the chor-
ioid gland, the argentea, and the usual vascular, pigmented connective
tissue, the Amia chorioid contains many small venous sinuses.

There is a very narrow ciliary zone between the ora terminalis and the
point where the uvea definitely bends away from the sclera to become

THE HOLOSTEAN EYE 575

the iris stroma. The uvea here contains no ciHary or Briicke's muscle;
but mid-ventrally there is a lens-muscle papilla or campanula. In Amia
this is large, and the pigmented lens muscle blends with a definite tendon
which in turn attaches to the lens capsule. In Lepisosteus the small
muscle attaches directly without a tendon; but there is a meridional
ridge (lacking in Amia) extending backward from the campanula about
one-fourth of the way to the posterior pole of the eyeball, along the
route of the old embryonic fissure. This ridge may be homologous with
the teleostean falciform process iv.i.), but this is not certain; nor is it
known for sure whether the holostean 'campanula' and lens muscle are
even identical in function with the teleostean structures (i. e., retractive,
rather than protractive like the selachian lens muscle), let alone hom-
ologous therewith and ancestral thereto. The lens is supported from
above by a squarish suspensory ligament (essentially a strap of tough
vitreous — cf. sturgeons), with a broad insertion (4.0mm., in Lepisosteus)
on the lens.

The iris is devoid of muscles. It bears meridional folds dorsally in
Lepisosteus (as in rays and a few teleosts) . Its anteriormost layer is the
mesothelium (v.s.), following which comes a thin argentea continuing
that of the chorioid, and a thick, pigmented stroma. The anteriormost
retinal layer is heavily pigmented throughout, but the posteriormost is so
only in the region where it is most exposed to light. Behind the annular
ligament (which is semi-opaque) its pigmentation fades, so that there is
a gradient from the pupil to the 'ciliary' region, where the innermost
epithelial layer is completely bleached as in all vertebrates.

In both genera, the vitreo-retinal boundary consists of a delicate,
presumably mesodermal membrane, in which is suspended a network of
small blood vessels. These Vitreal' or 'hyaloid'* vessels, first encoun-
tered here historically (but see p. 566, bottom) , are common in teleosts
and occur in some lungfishes and in amphibians, with imitations (of
entirely separate origins) in snakes and mammals. They are clearly de-
voted to the nourishment of the inner layers of the retina, and will be
discussed below in the paragraphs on the teleosts. In the holosteans, as
in the amphibians and some teleosts (catfishes), the large artery and
vein which supply the network enter the eyeball cavity at the mid-ventral
point of the ora terminalis.

*No connection with the hyaloid vessels of the fetal mammalian eye — see p. 113.

576 HIGHER FISHES

The Holostean Retina — The retina of Amia — except for its visual-
cell pattern — is quite in line with teleostean retinae histologically. The
lamina vitrea is particularly thick. The pigment-epithelial cells have long
processes reaching nearly to the limitans. These are fine and multiple,
so that the cell as a whole is structurally intermediate between those
shown in Figure 20d and 20e (p. 44). The horizontal cells form two
layers, those of the outer tending to be chunky parallelopipeds as in the
lowest fishes, but the inner ones ropy and seemingly on the way to be-
coming fibrous and 'conductive' in appearance like those of the higher
vertebrates (see p. 49). The bipolar and amacrine nuclei form the four
loose remaining rows of the inner nuclear layer. The outer nuclear layer
contains three ragged rows, the ganglion-cell layer a single scattered
row of nuclei. The visual cells are described in connection with those
of the teleosts (see Fig. 170b, p. 587).

The retina of Lepisosteus has never been fully described. Some vague
statements of Mary McEwan suggest however that it is very much like
that of Amia.

In both genera of holosteans the optic nerve is essentially circular in
cross-sectional outline, but its nervous substance is in the form of a
broad, thick ribbon which has been accordion-pleated edgewise to fit
it into a tubular sheath. Correspondingly, the optic 'disc' or nerve head
is not round, but vertically elongate as in many predaceous teleosts with
similarly high cone-to-rod ratios (see pp. 179-80).

Teleosts — Ocular structure in the chondrostean-holostean-teleostean
line culminates here in a pattern whose new features are of absorbing
interest from the physiological and ecological standpoints, but must be
studied purely for their own sake since they have not been passed on to
any higher groups. We can make only physiological comparisons be-
tween the teleosts and the amphibians. The origins of all peculiarly
amphibian ocular features must be sought far from these 'highest' fishes,
in the imperfectly-known chondrostean-dipnoan-crossopterygian series
of patterns.

The teleosts long ago split into two great lines : the malacopterygians
(soft-rayed fishes), in most of which the swim-bladder, an ancient lung,
remained open to the throat (hence the approximately equivalent name
'Physostomi' for these fishes) ; and the spiny-rayed fishes or acanthop-
terygians, all of which have the swim-bladder closed off, and belong to
the 'Physoclisti' along with a few groups — synentognaths (halfbeaks,
needlefishes), cyprinodonts (killifishes) , and the 'Anacanthini' (cods,

HOLOSTEAN RETINA; TELEOST EYE 577

grenadiers etc.) — which lack true spines (though the cyprinodonts, pos-
sibly also the anacanthines, are to be suspected of having once had them) .
Figure 169 shows all of the principal morphological features which
teleost eyes ever present, though of course not always with these partic-
ular sizes, shapes, and orientations. Each of these features may be present

scleral cortilage

chorioid
'gland'

epichorioidal lymph space

cornea:

autochlhon-
'ous layer

scleral
layer

dermal
, J ^ " layer

lent/form
body

orgenlea of/
chorioid

argentea
of iris

annular
ligament

conjunctiva
tensor chorioidece

Fig. 169 — Diagrammatic vertical section of typical teleost eye.

Certain of the structures may be lacking in a particular species (see text). A falciform
process and a system of hyaloid vessels are never simultaneously present; and where the
falciform process is lacking, the lentiform body is absent also. The argentea, shown in
black, actually of course contains reflective, not absorptive, pigment.

or absent, usually independently of any others, from family to family
or even within one family, without much regard to the families' taxo-
nomic positions. Particularly, there is no feature which may not be
present (or absent) in both malacopterygian and acanthopterygian

578 HIGHER FISHES

families. In other words, it appears that all of these special teleostean
structures had been evolved before the great schism came; and, though
in general the physostomes are anatomically a bit 'primitive' as com-
pared with physoclists, there is no majestic progress to be seen in passing
through the families of the one division to the families of the other.

The margin of the circumocular sulcus usually forms a narrow circular
lid-fold, lapping onto the eyeball. Where the eye is retractile, temporary
'lids' may largely cover the eye (sometimes moved by a special dermal
sphincter muscle, like an orbicularis) ; and 'adipose lids' (^.v.) are com-
mon in swift swimmers. The orbit is usually roomy unless the eyeball is
very large or tubular. Cushioning venous sinuses are developed to
greater or lesser degree, but other orbital structures are very variable
and our knowledge of them lacks synthesis. A tenacular ligament often
holds the eyeball in the orbit; this has no genetic relation to the selachian
optic pedicel, for in some rays both structures are present side by side.

The oculomotor muscles are usually normal in number and arrange-
ment (see Fig. 165, p. 565). They are often long, and are carried
through canals in the bones of the skull — an anterior canal holding the
two obliques, and a posterior one the four recti. There are no special
retractor- or levator-bulbi muscles.

The eyeball is almost always flattened anteriorly, with its axial length
its shortest diameter, and with its horizontal diameter tending to be its
greatest dimension in swift forms, but more nearly equal to the vertical
diameter in slow-swimming and small-eyed species. Since the corneal
surface is eliminated optically, there is no need for it to be smooth; and
it is often irregular, concentrically ridged, etc.

The sclera is very variable in its morphology. Primitively, it must have
contained a complete cup of hyaline cartilage as in all lower fishes. It
does contain at least some cartilage except in gymnotid eels, pearl-fishes,
and a few others (where it is entirely tendinous) and in the tetras (where
it is entirely bony) . But in no instance is the cartilage-cup intact fundally
— one might put it that the floor of the original cup, over the whole back
of the eyeball, has been replaced by fibrous tissue. This fibrous window
is often so large that the cartilage is restricted to a broad equatorial, or
narrow just-post-limbal, ring (e.g., pipefishes, many salmonids). The
cartilage may also be widely distributed, not as one piece but in the form
of little islands in a fibrous continuum (elephant-fishes) . Typically there
are thin plates of bone temporally and nasally, which may develop either
anterior to the cartilage or external to it (the cartilage beneath them

THE TELEOST EYE 579

then atrophying — e.g., minnows) — occasionally, jrom preformed car-
tilage {Salmo, Pagellus, Crenilabrus) . Both ossicles, only one, or none
may occur within one family (herrings), and both are lacking in many
small-eyed and bottom forms. Conversely, they may be enormous and
joined to form a complete ring in large, large-eyed, swift swimmers
(tuna, swordfish).

The cornea is also variable in make-up. Topographically, it is usually
broad, and it tends to depart from a circular outline in the direction
of a horizontally elliptical one, and to have its center shifted more or
less nasally. These tendencies are more pronounced in swift swimmers
than in slow ones, in marine forms than in freshwater species, and are
obviously purposed to enlarge the binocular field with a minimal sacrifice
of periscopy in the horizontal plane. Anatomically, the only constant
feature of the teleost cornea is the portion of the substantia propria
which is directly continuous with the cartilaginous and fibrous layers
of the sclera, and which may be designated the 'scleral' portion of the
cornea. External to this, and ordinarily fused with it, is an additional
mass of tendinous substantia propria representing the dermis of the skin
(see Fig. 151, p. 451), and bearing externally the (usually) thin corneal
epithelium. This 'dermal' part of the cornea and the scleral layer are
jointly homologous with the entire cornea in the chondrosteans and
elasmobranchs; but, unlike those 'more primitive' fishes, teleosts have
preserved a visible distinctness of the two layers, which moreover usually
expresses itself in a ready separability of them. Although this situation
would seem to be truly primitive — placing the teleost cornea between
those of the lampreys and the elasmobranchs — interestingly enough it is
particularly in some of the lower (physostome) teleosts that the sub-
stantia propria has become most nearly homogeneous and is no longer
easily peeled apart into dermal and scleral laminae (e.g., salmonids,
minnows, pikes).* The customary easy separability of the cornea has
an evolutionary aspect as well as an immediate mechanical one, for it has
led many times to the production of a 'spectacle' through a reversion to
the primitive cyclostome situation in which the skin was not joined to
the dural capsule of the eyeball.

*The homogeneity may be owing to the dermal propria's having actually disappeared from
between the epithelium and the scleral propria. This appearance is given, for example, by
the goldfish, where the dermal propria is either absent or consists at most of but a single
layer of collagenous fibers continuous with such a layer in the conjunrtiva. It may be that
variations in the elaboration of the general head dermis can reflea in the laminations of
the cornea.

580 HIGHER FISHES

A further major complication is introduced by the common or usual
presence of an 'autochthonous' layer or mass of coarse-fibered sub-
stantia propria. This is distinct from and internal to the scleral layer,
and always itself bears the thin Descemet's membrane and mesothelium
(lacking in pikes?) . Rarely, the scleral layer may be easily separable from
the autochthonous, and may even (e.g., Lepomis macrochirus) bear in-
wardly a mesothelium for all the world like a Descemet's, though with-
out any elastic, cuticular basement membrane. The phylogenetic origin
of the autochthonous layer cannot be traced. It looks as if it had been
formed in situ from 'nothing' (hence its name), magically interpolated
between Descemet's membrane and the scleral propria. At the periphery
of the cornea, the autochthonous layer usually thickens greatly, then
abruptly tapers to a knife-edge termination opposite the front margin of
the scleral cartilage or bone. Descemet's layers ordinarily do not extend
nearly this far peripherally, for the mesothelium is reflected over (or
forms) the annular ligament (see also p. 574) and continues back toward
the pupil on the anterior face of the iris.

In a few fishes, including gobies and particularly the plectognaths
(trunkfishes, puffers, ocean sunfishes etc.) the corneal substantia propria
exhibits a complex lamination, with histologically peculiar intercalated
layers which cannot be related at present to the typical lamination-
system just described.

The 'annular ligament' — an inappropriate name, but one for which
no good substitute has yet been offered — is almost universally present;
but it can be greatly reduced or lacking in species of a genus which
characteristically has it well developed (e.g., Anabas). It is no teleostean
monopoly, but was invented by fishes as archaic as the Chondrostei, if
not by the cyclostomes. The justification for calling it a ligament is the
fact that it gives the appearance of forming a bracket between cornea
and iris, holding them at a fixed angle to each other. Actually, the tissue
of the ligament is (always?) so very ductile that it can have no such
sustentative function. The ligament adds to the difficulty of defining
the boundary between the iris and the ciliary body in teleosts, for one
naturally tends to consider, as 'iris', only what is free of the annular
ligament. Actually, the greater part of the iris — best defined as the por-
tion of the uvea within the limbal circle — is covered by the ligament, and
the true ciliary zone (from limbus to ora terminalis) is very narrow.
Embryologically, the annular ligament arises from an accumulation of
mesodermal cells which lie at the periphery of, and continuous with, the

THE TELEOST EYE 581

Descemet's mesothelium of the cornea. Histologically, it is usually com-
posed solidly of swollen or polyhedral epithelioid cells; but it may be
loculated and vascularized (Periophthalmus) or dotted with melano-
phores and iridocytes (Gadus). In the bluegill, Lepomis macrochirus,
the whole of the ligament appears to be occupied by a single lymph
sinus (perhaps continuous with the epichorioidal one), which is criss-
crossed by mesothelial trabeculae. Where the tissue is solid and epithel-
ioid, the cells contain granules which are perhaps always of glycogen,
perhaps sometimes of other substances. The ligament then has a 'secre-
tory' look; but what it may secrete, in the fashion of an endocrine gland,
is a puzzle. It could conceivably be the source of either the whole of the
aqueous humor, or of solutes which raise the osmotic pressure of the
aqueous; but the ligament is no less well developed in freshwater teleosts
than in marine ones. Occasionally, stuffed between the cornea and the
annular ligament, or sometimes embedded in the latter (but never in
the cornea or sclera), there is a 'canal of Schlemm', which has connec-
tions to iridic or hyaloid vessels and is obviously not homologous with
the true Schlemm's canal of the sauropsidans and mammals.

The chorioid, in addition to the usual pigmented vascular layers,
choriocapillaris, argentea (usually) , and (occasionally) tapetum fibrosum,
characteristically contains the same 'chorioid gland' which we noted in
Amid — never as large, however, as there. It is ordinarily horseshoe-
shaped, though it sometimes forms a complete ring around the optic
nerve (some minnows), or may be divided in two parts as in one of the
sea basses (Labrax). Between the limbs of the horseshoe, ventral to the
optic nerve, there is a second body of the same histological sort — the
'lentiform body' — in some families and scattered genera.

The presence of the chorioid gland is rigidly dependent upon the
presence of a 'pseudobranch', the vestigial hyoid gill which is found on
the inner side of the operculum or gill-cover in most teleosts. The blood
which has been aerated in the pseudobranch is gathered into an efferent
artery which, in the neighborhood of the optic nerve, enters the sclera
and breaks up into a set of capillaries in the chorioid gland. From these,
the blood flows into the ordinary chorioidal circulation. In fishes which
have lost the pseudobranch for any reason, the chorioid gland is in-
evitably lacking also. In general, this is true of small-eyed forms —
catfishes, eels, characins, elephant-fishes, etc. In a similar way, the
lentiform body is interpolated in the arterial supply to the falciform

582 HIGHER FISHES

process, and is lacking where the process itself is absent (as well as in
many fishes which do have the process) .

The falciform (/. e., sickle-shaped) process is perhaps foreshadowed in
holosteans (Lepisosteus) , but it comes into prominence only in the tele-
osts. In its fullest development it is a ridge, formed of pigmented and
vascular chorioidal tissue, which projects upward into the vitreous cavity
from the floor of the eyeball. This protrusion of the chorioid through
the retina is permitted by the fact that the lips of the embryonic fissure
of the optic cup have never closed (see pp. 104-7). The falciform
process consequently runs ventrally from the optic nerve head, and also
veers nasally, tracing the course of the old embryonic fissure. Occasion-
ally it appears to commence above the optic nerve; but this 'dorsal ap-
pendix' of the process is always unpigmented and lies on the retina,
never projecting through it from behind.

There are great variations in the form and extent of the falciform
process. It may be tall either proximally or (particularly, in physostomes)
distally, or may be low throughout its length (most physoclists) . In the
needlefish, Be lone, it is so tall and thin that it forms a partition in
the whole ventral half of the eyeball, running from fundus to iris with
contact on the lens over a full half-circle, and serving (through its
elasticity) as the quick-acting antagonist of the muscle of accommo-
dation in this agile fish. The process, if reduced in longitudinal extent,
is always present distally (i.e., toward the ora terminalis) and absent
proximally (toward the fundus). Never does it commence at the optic
disc and run only part-way to the ora; for any partial healing of the
embryonic fissure in the sensory retina (tending to shorten the falciform
process) always has a proximal-^distal direction.* Instances in which
the length of the process is thus somewhat reduced include the stickle-
backs, wrasses, blennies, some cods, and some herrings. It is present only
near the ora in minnows, pipefishes and sea-horses, clingfishes, the sprat,
and the (American) pollack. Thus, there may be variations within a
family (e.g., Clupeidx, Gadidae).

Where the falciform process is wholly lacking (e.g., elephant-fishes,
eels, trunkfishes and puffers, anglers and batfishes), and in some in-
stances where it is present but only far distally, there is a system of

* Since the definitive vitreous of vertebrates is always secreted by the sensory retina, it has
a slit-like defect in teleosts — the 'vitreous cleft' — above the falciform process, which locally
prevents such secretion (see Fig. 105a, vc; p. 261).

THE TELEOST EYE 583

hyaloid vessels clinging to the inner surface of the retina (see also
p. 575). These are usually supplied from the same artery which would
otherwise go to the falciform process; but when the latter is absent the
artery enters the vitreal cavity at the disc, and branches over the retina,
instead of turning ventrally there to run through the chorioid along the
line of the embryonic fissure. Falciform process and hyaloid vessels are
thus mutually exclusive — a given teleost exhibits one or the other in
full bloom, never both. Since the vitreal vessels are clearly concerned
with the nutrition of the inner layers of the retina, it may be assumed
that this is also the primary or sole function of the falciform process,
from which nutrients {e.g., glucose) could readily diffuse in all direc-
tions through the vitreous, to be absorbed therefrom by the retina. When
in later chapters we compare the snakes with the lizards, and the mam-
mals with the birds, we shall find in each case an exactly comparable
situation: a mutual exclusiveness of two very different mechanisms for
the nourishment of the nervous layers of the retina (see pp. 648-58).

At the distal end of the falciform process lies the 'campanula Halleri'
or retractor lentis, with its ectodermal muscular elements and its pig-
mented investment derived respectively from the inner and outer layers
of the blind retina. Occasionally very small or wholly lacking {e.g.,
eels, gadids), the muscle when well developed still shows great variabil-
ity with regard to size, shape, orientation, presence of tendons (derived
from vitreous material) at one or both ends, etc. It pulls directly upon
the subspherical lens (which is suspended pendulum-fashion from a
dorsonasal suspensory-ligament thickening of vitreous) , drawing it back-
ward and temporad. This accommodatory apparatus, like the falciform
process, may actually have been invented by the holosteans — possibly
even by the chondrosteans {q. v.) ; but it is characteristically teleostean,
and no semblance of it occurs in the land vertebrates or in the groups
of fishes leading toward them (see next Section). The absence of the
falciform process does not affect the presence of the campanula, though
this, when a falciform process is present, is usually attached thereto; and
the nerve and artery which supply the muscle emerge from the distal
part of the process. The two structures sometimes cooperate particularly
well, as in the mackerel {Scomber scombrus), where the falciform process
lifts completely free of the retina and holds the campanula up to the lens.

The narrow ciliary zone of the uvea contains a few meridional muscle
fibers, simulating closely the 'muscle of Briicke' which accomplishes ac-
commodation in the Sauropsida and mammals. In teleosts, the ana-

584 HIGHER FISHES

tomical name which expresses its function (?) is 'tensor chorioideae'.
Though it is absent in those teleosts which have no accommodation, it
is not directly concerned in that process — rather, it seems to serve to
tauten the chorioid and retina around the vitreous body, thus preventing
the backward-moving lens from using the vitreous to push the retina
backward, which would defeat the accommodatory purpose of the re-
traction of the lens. This function of the muscle has never been estab-
lished experimentally, however; and, strictly, its usefulness must be
regarded as unknown.

In the ciliary zone, the chorioid merges imperceptibly into the true
iris, which is fairly complex in structure. Typically, there is an anterior
layer of mesothelium, continuous by way of the annular ligament with
that of the cornea. Behind this is a thick argentea continuing that of the
chorioid. The pigmented and very richly vascular stroma posterior to
the argentea bears, superficially, a scattered layer of chromatophore cell-
bodies whose processes perforate the argentea and expand within it, or
more often anterior to it (beneath the mesothelium) to contribute to the
externally-visible color pattern of the iris as a whole. The anteriormost
of the epithelial retinal layers of the iris is always heavily pigmented
except toward the pupil where it is converted into the lightly pigmented
(sometimes unpigmented) 'sphincter'. The posterior retinal layer is pig-
mented only in the pupillary half of the iris, and is blank behind the
annular ligament as in the ciliary zone. Between the stroma and the
retinal layers there is a conspicuous membrane which gives one the im-
pression of a myoid dilatator-sheet (as in the mammals — see Fig. 7b
and g, p. 15) ; but this membrane is only a basement-membrane, com-
parable with the glass membrane in the region of the sensory retina —
any dilatator elements ever present in teleosts are pigmented spindle-
shaped cells, detached from the epithelium and lying in the stroma. The
sphincter, when present, is not so well separated from the generative
epithelium as it is in mammals. Very often a 'sphincter', sometimes a
massive one, is present without demonstrable contractility. The vascular-
ization of the iris is complex and variable, and its different plans in
different groups have yet to be fully interpreted and unified; but the
uncertainties here, in this blind-alley group of vertebrates, are of no
consequence to the phylogenetic theme of these synoptic chapters.

The Teleost Retina — In so huge and diversified a class of vertebrates,
the retina naturally shows great differences from one group to another.
The fishes of the caves and crevices, muddy waters, and the deep sea

THE TELEOST RETINA 585

have been dealt with in the ecological chapters. Here, we can only
generalize about the retinae of the more ordinary teleosts, taking a
little space to mention a few of the more outstanding departures from
standard conditions.

The retina in teleosts varies more in thickness than in other vertebrate
classes, from less than 100[1 to more than 500|1. Much of this variation
is caused by variation in the number of conductive elements per num-
ber of visual cells; but an unusual proportion of the thickness is usually
occupied by the visual-cell + pigment-epithelial layers, owing to the need
for scope for the extensive photomechanical changes characteristic of
the group. The other layers exhibit a neatness and 'purity' {i.e., an ab-
sence of ectopic elements) which we shall not see elsewhere until we
reach the lizards, birds, and mammals. The horizontal cells usually have
small bodies and slender (conductive?) processes, but occasionally —
and not only in physostomes (e.g., Esox) but even in the 'highest' tele-
osts {e.g., Stizostedion, a percid) one encounters massive, stellate hori-
zontals with broad bodies and short, thick, anastamosing processes —
exactly like those of some of the lowest fishes. Where the cones are pre-
dominant, the piling up of conductive and integrative elements results
in a thick inner nuclear layer and a compact ganglion-cell layer. At the
other extreme is the situation in such a light-shunning fish as the bull-
head, Ameiunis nebulosus, where the rods are large and the cones few
and small (see Fig. 63, p. 147). Here, the outer nuclear layer contains
only two rows of nuclei, the inner nuclear layer but one; the ganglion
cells are widely scattered, and only 2/9 of the thickness of the whole
retina lies between the external and internal limiting membranes.

The cells of the pigment epithelium are usually long, with most of
the length contributed by their processes, which are few but thick, and
reach nearly (or quite) to the external limiting membrane (Fig. 20e,
p. 44). The migratory fuscin is usually in the form of needle-shaped
granules, the stationary pigment in round granules. Guanin may also
be present in large amounts, as in those minnows and perches which
have evolved occlusible tapeta lucida, and also in many deep-sea fishes
and in the Mormyridae, Elopidae, and Thunnidse, some anchovies, some
mackerels, the louvar, and one serranid {Polyprion) .*

*These were not included in Table VII, pp. 240-1, as having effective tapeta, since the
presence of pigment as well as guanin in some of them (together with the absence of any
pronounced photomechanical changes) makes it questionable, without further study, how
effective the guanin may be as a mirror.

586 HIGHER FISHES

In nearly all teleosts there are three types of visual cells : rods, single
cones, and the twin cones which the teleosts monopolize (Fig. 170).
In a particular retina, or in particular regions in some retinae, only one
of these, or any two of them, may occur. The pure-rod teleosts include
the deep-sea forms and (according to Verrier) one siluroid, Clarias
batrachus* Twin cones alone occur in Pollachius pollachtus and some
Gadus spp.,"*" in Scorpcena porcus, Sebastodes elongatus, Alosa finta,
and in all but the extreme periphery in a number of others — particularly
flatfishes and swift surface forms (tunas, mackerels, mullets, etc.). The
relative numbers of twin cones (where they are mingled with singles
and with rods) decrease with an increase in the species' preferred depth
of swimming. Clearly, the twin cone is associated with exposure to
bright light.

The origin of the twin cone cannot be traced with certainty. It usually
looks so much like two single cones fused together that this simplest
explanation is the one dictated by the law of parsimony (see Plate I).
But the holostean visual-cell assortment looks superficially much like the
teleostean. Here (Fig. 170b) there are rods, single and double cones.
The teleostean twin might have arisen from the holostean double through
an equalization of the latter's two members, involving the loss of the
accessory's paraboloid (the chief cone's oil-droplet being already long
since gone in Amia, and replaced functionally there by a yellow cornea).
Supporting this possibility is the fact that double cones, of sorts, do
occur in teleosts — that is, conjugate elements whose two members are
unlike in size and, to some extent, in structure. The oldest report of
such elements is that of Greeff, who described them for Rutilus rutilus
in 1900. The writer has found the conjugate elements of the goldfish
(Carassius auratus) to be of this same sort. Rutilus and Carassius are
both members of the minnow family (Cyprinidae), which stands rather
near the bottom of the malacopterygian division. The Salmonidse rank
about as low or lower; and Mile. Verrier and Miss McEwan have de-
scribed doubles, or unequal twins, for Salmo gairdnerii irideus and S.
trutta fario. The occurrence of so many instances of unequal twins

*A dubious observation, for a few years later she reported rods and single cones, in equal
numbers, for Clarias dussumien.

fTending to throw doubt upon the coryphsenoidid ancestry of the cods (see pp. 389-9),
since for the cods to have had pure-rod ancestors, and yet possess twin cones, would neces-
sitate believing that they had invented twin cones for themselves. Still, the absence in gadids
of accommodation and of scleral ossicles, together with the particularly easy 'splittability' of
their comese, suggests that these fishes may well have risen secondarily from the ocean floor.

THE TELEOST RETINA

587

among the most primitive of living teleosts makes it seem fairly reason-
able that the typical identical-twin cones of teleosts have indeed been
derived from double elements like those of Amia. Against this view,
however, must be placed the presence of double cones in Fundulus (see
Fig. 24f, p. 59). Fundulus being one of the cyprinodonts, which (though
they are soft-rayed physoclists) probably deserve a place near the perches
at the top of the acanthopterygian heap, its double cones may well have
been manufactured from ancestral typical twins. And if this has been

CD

O

CO

ocoo

0

oO

ocoo

Po

03

Fig. 170 — Visual-cell patterns of holosteans and teleosts.

a, units of visual-cell mosaics in representative teleosts. Redrawn from Eigenmann and
Schafer. Only the single and twin cones are shown — the (much smaller) rods fill the spaces
around and among them; from above downward: commonest pattern, as seen in Perca;
pattern in Salmo (without the central single, this would represent Blennius); pattern in
Scorpana porcus.

b, single cone, double cone, and rod of a holostean, Amia calva. x 1000.

c, single cone, twin cone, and rod of a teleost, Sli;osleJtori vitretnn. xlOOO. Drawn from .1
preparation of George A. Moore.

588 HIGHER FISHES

possible once, it may have been possible many times, and secondary
derivation from twins may thus account for all teleostean 'doubles'.

The visual cells are nearly always arranged in a neat mosaic; and
where this is true, the unit of the mosaic is almost invariably a perfect
square, with a twin cone on each side (Fig. 170a).* In some instances,
where the visual cells are particularly large {e.g., Fig. 170c), the mosaic
is visible ophthalmoscopically in the living animal Where the rods are
very small and very numerous, as they usually are, they often occur in
clusters or bouquets, with their myoids of unequal length so that the rod
mass is pseudostratified — there being no room for the rods all to be
brought into a single plane even in either extreme dark- or extreme
light- adaptation. In two families — the elephant-fishes (Mormyridas) and
the ten-pounders (Elopids) — both rods and cones are gathered together
into great bunches, each surrounded by the heavy conical processes of a
circle of adjacent pigment-epithelial cells. In many teleosts, the cone
nuclei lie partly or wholly through the external limiting membrane, and
are much larger and less stainable than those of the rods (c/. Fig. 94,
p. 237). The foot-pieces are then very different, those of the cones being
heavy and dendritic while those of the rods are filamentous and termi-
nate in tiny smooth end-knobs. These differentiations of nuclei and foot-
pieces do not occur below the teleosts; nor do they appear on the land-
animal side of the fence until the amniotes are reached. Though the
physiological meaning of these differentiations is obscure, the sharing of
them by the teleosts, birds, and placental mammals seems definitely
correlated with the presence, in these same groups, of species having
such things as extensive accommodation, high visual acuity, brief biolog-
ical moments, fovea, and color vision. The teleostean eye and retina,
at their best, are outstanding in 'perfection' among all the fishes, and
represent the fishes' nearest approach to the ocular quality of the very
highest vertebrates.

(D) Cladistians and Dipnoans

These are the living 'lunged' fishes — though by no means the only
ones which ever use the swim-bladder for breathing air at the surface.
The two living cladistian genera, Polypterus and Calamoichthys (both
inhabiting African rivers), were formerly classed as crossopterygians,

^Obviously, it would be decidedly worthwhile to make tangential sertions of the retin* of
Amid and some of the Gadidae; for if the conjugate elements of these forms are found to
be arranged also in squares, our ideas about the origin of twin cones may be clarified.

CLADISTIAN AND DIPNOAN EYES 589

but cannot now be considered at all close to the roots of the amphibian
stock. The lungfishes strictly speaking (Dipnoi or Dipneusti), repre-
sented only by Protopterus, Lepidosiren, and Neoceratodus (living re-
spectively in African, South American, and Australian rivers) , are not
too close to the amphibians either. The latter arose from the Cross-
opterygii, which were offshoots from an extinct dipnoan line. But unless
and until the eye of the newly-discovered sole living crossopterygian
fish, Latimeria chalumnce, is sometime described, we have only the dip-
noans to indicate to us how the amphibian eye may have evolved from
its ultimate chondrostean ancestor (see Fig. 60, p. 135). The cladistians
may be expected to be of some help also, for their connection with the
chondrosteans is very close to the stem of the dipnoan-crossopterygian
line.

Cladistians — Nothing is known concerning Calamoichthys, and the
eye of Polypterus has had no more complete studies than the sketchy one
of Leydig in 1854. The sclera exhibits the usual piscine hyaline-cartilage
cup. In the chorioid there is a silvery layer, but it is unclear whether this
is a guanin tapetum lucidum or an argentea (see p. 240). There are
vitreal vessels, with their main vascular supply coming in at the mid-
ventral point of the ora as in Amid and amphibians (suggesting that
the primitive chondrosteans may have had such vessels — see Fig. 60).
There is no trace of any mechanism of accommodation. The retina is
quite unknown; but the optic nerve has been described as having a num-
ber of branches, so that the optic papilla is multiple (see p. 367) .

Dipnoans

See also pages:

135-6 Fig. 60, taxonomy, anatomy 200, 216-7 visual cells, oil-droplets

150, 160, 220, 222-3 pupil 263-4, 216-7 accommodation

187 lack of area centralis 525, 537 dermal color changes

Only the eye of Protopterus has been given any complete descriptions
(by Hosch in 1904, Grynfeltt in 1911), and these have been faulty.
All three genera are said to have nothing like a falciform process, and
no accommodatory structures. There is of course no canal of Schlemm.
Lepidosiren is claimed to lack the oblique muscles; little is known about
its eyeball. The dearth of knowledge about Lepidosiren is of no great
importance, since this form is in the same family as Protopterus. But
Neoceratodus deserves a thorough investigation, for this large fish has
none of the appearances of degeneracy characteristic of the Lepido-

590 HIGHER FISHES

sirenidae. Its relatively large eye may have, in particular, a mechanism
of accommodation; and its cone oil-droplets may be colored in life. But
the animal is reputedly nocturnal (in captivity, at least), and may not
have retained such things even though some diurnal ancestor may have
had them. Neoceratodus (and Latimeria) remain our chief hope of ever
learning the origin of the amphibian mechanism of accommodation,
which is so distinct from those of all known fishes. Unless otherwise
noted, the following statements apply only to Protopterus icethiopicus) :

The ca. 2.0mm. eyeball turns freely under a transparent dermal 'sec-
ondary spectacle' (Lepidosiren also) . The cup-like scleral cartilage, which
is about two cells thick, reaches only to the equator of the eyeball; but a
fibrous continuation of it becomes, anteriorly, the inner portion of the
cornea. The fibrous layer of the sclera external to the cartilage also
continues forward as a portion of the corneal substantia propria, entirely
unconnected with the skin of the spectacle (and apparently separate, or
at least very readily separable, from the inner moiety of the cornea).
The Descemet's membrane and mesothelium are the thinnest imaginable.

The chorioid consists of little more than a choriocapillaris, with only
wisps of connective tissue, containing a very occasional pigment cell —
altogether the thinnest, simplest chorioid outside of the blind vertebrates.
There are no traces of a chorioid gland or of an argentea. The circu-
latory pattern of the eye includes a set of vitreal vessels (not in Neo-
ceratodus— hence there, perhaps, a falciform process?) .

The iris departs directly from the ora terminalis without the inter-
calation of any zone which could be called ciliary, and without support
for its root in the form of any pectinate ligament or mass of meshwork
tissue in the angle between it and the cornea. It is very thin — its stroma
thinner than its retinal layers. Even the latter appear to have tried to
thin out, for the pigmented anterior layer is squamous rather than
cuboidal as usual. The posterior retinal layer is nearly free of pigment,
so that the iris (and indeed, the whole eye) is as simple as that of a
brook lamprey. The relatively huge (1.16mm.) lens lies entirely behind
the iris, so that the pupil is free to change in size; and it can do so, in
Protopterus at least, despite the total absence of any discernible mod-
ification of iridic cells into myoepithelial elements.

The Dipnoan Retina — Here again, little can be said about Neocer-
atodus, and not much more about Lepidosiren. In the latter and in Pro-
topterus, the pigment-epithelial cells are huge, the epithelium being as
thick as the sclera and much thicker than the rudimented chorioid.

THE DIPNOAN RETINA

591

r^

The processes are numerous, long, and filamentous (Fig. 20d, p. 44).

All of the retinal elements are monstrous, as are the cells in most of
the organs of lepidosirenids. In Protopterus the outer nuclear layer con-
tains two rows, each incomplete — more nuclei lie above the excessively
delicate limitans than below it, and both rod and cone nuclei may occur
in either location. The inner nuclear layer consists of four compact rows;
and if horizontal cells are present, their cytosomes are as slenderly fibrous
as those of the highest vertebrates. The outer plexiform layer is extreme-
ly thin, the inner plexiform thick as usual. There is a single
row of ganglion cells. The optic nerve of Protopterus is a
slender and simple cord, with an ependymal core as in lam-
preys; but in Lepidosiren and Neoceratodus the nerve fibers
are blocked off by glial septa into fascicles, each with an
axial core of (ependymal?) nuclei.

Protopterus has the most elab-
orate visual-cell pattern (Fig. 171
and Plate I). The rod exhibits a
maximum of cone-like morpholog-
ical features: it not only has the
same cone-like (i.e., particulate)
nuclear chromatin as the rods of
most lower vertebrates and the
cones of all, but it also has a huge
oil-droplet and a paraboloid (cf.
Figs. 22, 23; pp. 54-5). This rod
has certainly been secondarily de-
rived from a cone, and the chances
are that it is archaic, and represents
the primitive chondrostean rod,
changed but little or not at all.
On the pathway leading toward the teleosts this rod promptly lost its
oil-droplet (as did the cones at the holostean level, where the light-loving
Amia has had to replace them with a yellow cornea) ; but here in the
lungfishes the oil-droplet has persisted. There remains of course a possi-
bility that the lungfish rod has been derived from a lungfish single cone.

In Lepidosiren, according to Kerr, there are only elements which seem
identical with the rods of Protopterus. Neoceratodus, according to the
half-century-old observations of Schiefferdecker, has only single cones
with oil-droplets and rods without them.

Fig. 171 — Representative visual cells of
African lungfish, Protopterus athiopicus:
single cone, double cone, and rod. x 1000.

Chapter 15
AMPHIBIANS

See also pages: 257, 265-8, 272-3, 407, 436 accotnmo-
53-60, 176-7, 216-7 visual cells 'Nation, refraction

101 Fig. 33 274 scleral bone

102 Fig. 36 293 visual fields
105 Fig. 37a ^^^ ^^^ movements
109 regeneration of retina 3^9-40 median eyes

118 embryology ^44 movement-perception

123 Fig. 49a 367 optic nerve

134-9 origin, relationships ^75 lens and ultraviolet

145, 164, 208, 344, 368 habits 407 aquatic adaptations

146-53 photomechanical changes 415 thick sclera

148 Fig. 64, retina 421 Fig. 143a

150, 157-8, 161, 218-21, 223-4 pupil 428-9 comparison with elasmobranchs

184, 187, 305 area centralis 436 amphibious adaptations

193-6 value of oil-droplets 446 lens epithelium

200-2 oil-droplets 450, 453, 458 spectacles

210, 300, 390, 407, 458 cave salamanders 490-4, 518-9 vision, color vision

230, 240 eyeshine, lack of tapetum 525-8, 535-40 dermal color changes

251 Fig. 99 543-9 coloration of eye

In the fishes, the only important property of the cornea is its trans-
parency to light (and, perhaps, to water). But when the vertebrates
took over the dry land, the cornea at once presented advantages and
disadvantages, which had to be dealt with. To remain transparent, suc-
culent, and safe from injury, it had to be moistened by new glands and
wiped and shielded by lids (see also pp. 418-9). In exchange for these
attentions, the cornea offered the eye an opportunity to improve its
methods of operation : the outer surface of the cornea, now exposed to
air, became an important refractive surface. Some of the burden of focus-
ing the image on the retina being thus taken off of the lens, the latter
could now recede behind the iris. It then became easier to give the pupil
extensive mobility; and, the lens being brought into the plane of the
ciliary body, it became possible to discard lens-moving muscles and in-
stead use the ciliary muscle for accommodation.

If the fishes had attempted to obtain these benefits, the withdrawal
of the lens deep into the eyeball would have disastrously restricted the

592

THE ANURAN EYE 593

visual field. But once the cornea and lens became able to embrace a
wider cone of light-rays than the lens alone, there was no longer any
need of having the lens placed as far forward in the eye as possible.

The Amphibia have never felt fully the penalties, nor completely
realized the possibilities, in this situation. Their palpebral and glandular
complexes have not had to be brought to the perfection demanded of
the dry-skinned vertebrates; and they have clung to a lens-moving meth-
od of accommodation — indeed, one which they developed themselves —
without having ever developed the ciliary body to such a degree that it
could bear upon the lens and directly squeeze it.

The three living orders of amphibians are not closely inter-related.
The origin of the caecilians is quite unknown. The anurans and urodeles
are usually held to have had separate origins from stegocephalians; but
a modern theory, for which support is slowly growing, holds that the
urodeles were derived directly from lungfishes. We shall find no ophthal-
mological reasons for considering the urodeles any closer to the lung-
fishes than the anurans; and we shall see that since the two groups share
a number of new features — among them, such things as 'green' rods,
retractor bulbi and protractor lentis muscles, discontinuous ciliary mus-
cles, and fibrous zonules — there are good reasons for considering the
tailed and tailless amphibians to have had common ancestry after all.
Neither group can be called more primitive than the other; but the
Anura are treated first here because their eyes are a little more complex,
making it easy to describe the salamander eye largely by saying what
anuran features it lacks.

(A) Anurans

According to Noble, the tailless amphibians comprise ten families in
four suborders. The ocular structure of only two families — the Ranidae
(common frogs) in the highest suborder (Diplasiocoela) , and the Bufon-
idas (common toads) in the next highest (Proccela) — can be considered
well worked out. Future researches on other families may alter some of
the generalizations below.

The Eye as a Whole — At the time of metamorphosis from tadpole into
adult, the lids and 'nictitans' develop; and the aquatic, benthonic tad-
pole's dermal spectacle then fuses with the primary dural cornea, except
in the tongueless toads of the primitive family Pipidas* and in one or

*Xenopus, however, has a niaitans-Iike lower lid— chough no upper.

594 AMPHIBIANS

two bufonids which are hkewise permanently aquatic. The only massive
gland present is the Harderian, which, like the other 'terrestrial' features
(lids, nasolacrimal duct, flattening of lens, fusion of cornea and skin)
develops during metamorphosis, and forms most of the packing for the
eyeball in the largely membranous orbit. A broad and powerful retractor
bulbi muscle — probably evolved by the bifurcation of the external rectus
— is present, along with the six standard eye-muscles and a levator bulbi

Fig. 172 — The anuran eye in vertical section; semi-diagrammatic; based largely upon
the leopard frog, Rana pipiens. x 1 1 1^ .

ac- area centralis; to- inferior oblique; »V- inferior rectus; //- lower lid; Im, Im- lens muscles
(cf. Fig. 173); n- optic nerve; nm- 'nictitating membrane'; pn, pn- pupillary nodules; sc-
scleral cartilage; so- superior oblique; st- superior rectus; «/- upper lid; z- zonule.

Stolen from the chewing-muscles. The retractor is of aid in swallowing
food, as well as in the protection of the eyeball.

TTie eyeball is almost a perfect sphere, and has a deep anterior chamber
owing to the arching of the cornea and the recessed position of the lens
(Fig. 172). The curvature of the cornea blends smoothly into that of
the sclera, but is sharpened at its apex. During or after metamorphosis,
the fibrous sclera develops an extensive cup of hyaline cartilage, covered
externally by conneaive tissue which reaches forward, beyond the rim of

THE AN V RAN EYE

595

the cup, to maintain continuity with the substantia propria of the cornea.
The cartilage cup is usually thickest in the proximity of the optic nerve,
and terminates anteriorly a little ahead of the rectus insertions. It is less
extensive in this direction in Bnjo than in Rana, Pelo bates, and Alytes.
It is soft and perforate in Discoglossus, discontinuous in some hylids
(common tree-frogs), and lacking in at least one of them (Pseudacris,
whose sclera is entirely fibrous, at least in the adult) . In one microhylid,
Hypopachus incrassatus, a bony ring replaces the cartilage anteriorly.
The cornea is very broad, and has a ca. five-layered epithelium and a

Fig. 173 — The ventral ciliary process and associated structures in a frog, Rana pipiens. x 50.

c- cornea; ce- ciliary epithelium; cm- ciliary muscle; cp- ciliary process; cs- canal of Schlemm;
»'- iris; /- limbus cornea»; plm- protractor lentis muscle; r- sensory retina; s- sclera; c, Z-
zonule fibers.

homogeneous substantia propria — both, thinner apically than peripher-
ally. Both Descemet layers can be made out, though they are very thin.

The chorioid, apart from its choriocapillaris layer, consists largely of
two pigmented membranes held apart by numerous broad, flat, pig-
mented stmts, and enclosing between them a system of flat veins which
tend to have parallel, vertical courses. The outer surface of the chorioid
lacks an argentea, but may bear patches of xantholeucophores, guanin-
fiUed iridocytes, etc., which show through the translucent sclera.

The ciliary body occupies a narrow zone and (in section) is essen-
tially triangular, with the base of the triangle against the sclera just

596 AMPHIBIANS

behind the limbus. The posterior side of the triangle is faced with the
usual two-layered ciliary epithelium, and distally bears nearly a hundred
low folds, which continue meridionally onto the back of the iris. In
Rana, these iris folds run nearly to the pupil; but in Bufo they go only
half-way, and are lacking mid-dorsally and mid-ventrally (except for the
two 'ciliary processes'). From the posterior, plicate face of the ciliary
body, discrete cuticular fibers fan out to constitute a zonule; but these
are embedded in vitreous, which fills what would otherwise be the pos-
terior chamber. Mid-ventrally, a single prominent fold — large enough
to be called a 'ciliary process' — runs from the ora terminalis to the pupil
and there terminates in the ventral pupillary nodule (Fig. 172). Mid-
dorsally, two or three large folds are approximated, and aligned with a
dorsal pupillary nodule (possessed by most anurans in addition to the
ventral one; exception: Rana temporaria) . The zonule fibers stemming
from these heaviest uveal folds are the most important for the suspen-
sion of the lens, and transmit the force which protracts it in the act of
accommodation.

The anterior face of the ciliary triangle, bounding the anterior cham-
ber peripherally, runs from the limbus (or, dorsally and ventrally, from
the sclera behind the limbus) to the root of the iris, and is supposedly
covered by a continuation of Descemet's mesothelium (which, however,
if present at all, is in the form of a discontinuous patchwork). The
central area of the triangle is filled by a meshwork of vascular and pig-
mented connective tissue', forming a pectinate ligament of a sort. At the
base of the triangle, against the sclera, lie two structures which can best
be seen in vertical sagittal sections of the eye : the ciliary muscle, and
the canal of Schlemm. Neither of these forms a complete annulus around
the anterior segment as in higher vertebrates, but both the muscle and
the canal take the form of a dorsal-ventral pair of crescents, with gaps
between their horns nasally and temporally. Each canal has connections
with iris veins and, through the sclera, with conjunctival veins and
arteries. Their comparability with the Schlemm's canals of higher verte-
brates is most dubious; and even their function is in doubt, since they are
often widely separated from the anterior chamber and the aqueous which
they might be presumed to drain from the eyeball. Equally puzzling are
the dorsal and ventral ciliary muscles. These contain meridional fibers,
in some species circular ones as well. The meridional fibers run along the
inner surface of the sclera to insert in the chorioid; but it is difficult to
see, considering their location, what these muscles can accomplish. They

THE ANURAN EYE 597

are credited in the literature with having been demonstrated, by elec-
trical stimulation of the eye, to move the lens forward; but a little read-
ing reveals that these experiments were made (by Beer) long years before
the Russian anatomist Tretjakoff discovered the actual protractor lentis
muscles. Since the accommodation of amphibians is 'positive', not 'neg-
ative' as in the teleosts, any use of the ciliary muscles as a 'tensor chor-
ioideae' (see p. 584) would seem only to interfere with accommodation.
And yet, they are present in the sectors occupied by the accommoda-
tory muscles:

The actual (or important) muscles of accommodation are two, a
ventral and a dorsal (Figs. 172, 173, pp. 594, 595). They are of meso-
dermal origin embryologically, with no phylogenetic relationship to any
muscles outside the Amphibia (though they are supplied by a branch of
the oculomotor nerve, like the ectodermal teleostean retractor lentis).
Each runs from the periphery of the cornea through the iris root (the
ventral one passing through the old embryonic fissure) to insert within
the ciliary 'triangle' near its posterior face, in the body of the median
ciliary process. Their action is to draw forward these important anchor-
ages of the zonule, and thus approximate the lens to the cornea. The
large, firm lens is somewhat flattened, more so anteriorly than posteriorly.
The ratio of its equatorial to its axial diameter is about 1.3 :1 — a direct
optical consequence of the fact that the cornea, unlike that of a fish, is
able (in air) to share in the production of the retinal image. This flat-
tening is brought about ontogenetically just when it is needed; for the
tadpole lens is spherical, and lies closer to the cornea as well, in close
imitation of the optical situation in fishes.

In the iris, the stroma is thinner than the retinal layers — there is just
enough of it to hold the blood vessels together; and some of the latter
protrude through the anterior mesothelial 'layer' and bulge from the
surface of the iris, almost free of it. The stroma contains iridosomes as
well as melanophores, but there is no argentea layer. Both retinal layers
are pigmented. The cells of the anteriormost are drawn out radially into
spindles and constitute the dilatator pupillae. This is lacking only in the
region of the small, pigmented sphincter (beneath which the anterior
layer is said to be continuous, as unmodified epithelium, to the pupil
margin where it joins the squamous posterior retinal layer of the iris).
Around the pupillary nodules, whose function is to lift the iris free of
the lens to permit the surge of aqueous during accommodation, there
are special arrangements of the retinal and uveal tissues. In some forms

598 AMPHIBIANS

with horizontal pupils (bufonids particularly), the nodules are large
enough to meet when the pupil is fully contracted (see Fig. 87c, p. 223).

The circulation of the eyeball is complex, but because of the wide use
of the frog in zoological teaching, we should perhaps consider it in some
detail. As in 'ganoids' and in larval teleosts (before their pseudobranchs
have differentiated), its main arterial supply is from a branch of the
carotid, the 'ophthalmic artery', which on approaching the eye gives off
two branches. These puncture the sclera above (or within) the verti-
cally-ovoid disc, then diverge nasally and temporally in the chorioid to
feed the choriocapillaris. The dorsal halves of both chorioid and ciliary
body are drained by two veins which pass out through the sclera and
unite as the superior bulbar vein. The ventral halves drain centripetally
into a chorioidal venous 'star' from which an 'ophthalmic vein' leaves
the sclera posteriorly to join the internal jugular.

The main trunk of the ophthalmic artery enters the sclera ventro-
temporally and runs through the chorioid to the mid-ventral point of
the ciliary body, where it gives off two branches and then turns back-
ward onto the inner surface of the retina as the 'hyaloid artery'. The
two aforementioned branches anastamose around the root of the iris to
form a sort of major circle. From this, radial branches set up a plexus in
the pupillary zone of the iris, which drains through radial veins (in the
iris folds) into a venous rete in the ciliary body. This in turn is con-
nected with the veins of the chorioid.

The hyaloid artery (v.s.) bifurcates nasally and temporally, these
branches forming a nearly complete ring which lies just in front of the
ora terminalis (Fig. 172, p. 594). Meridional vessels given off from this
ring ramify backward over the retinal inner surface to generate a plexus
of 'vitreal' vessels. These recombine into veins which assemble into nasal
and temporal trunks (paralleling the arterial ring), and these in turn
join with a mid-ventral trunk to form the 'hyaloid vein', which turns out
through the chorioid alongside the hyaloid artery, and joins the ophthal-
mic vein (v.s.) .

The Retina — The anuran retina is characterized by large, coarse ele-
ments reminiscent of those in Protopterus (see Fig. 64b, p. 148). It has
the usual layers, and these have average thicknesses relative to each
other. The horizontal cells have as fine fibers as the bipolars, and are
apparently entirely conductive. The visual cells are thick in ranids,
longer and more slender in bufonids and hylids in keeping with the
nocturnality of the latter groups. They are of four types: single and

THE ANURAN RETINA 599

double cones, ordinary ('red') and 'green' rods (Figs. 64b, 174a). The
foot-pieces of all four types are dendritic, and their nuclei also 'cone-
like' (as to chromatin distribution). The red rods have their nuclei in
contact with the external limiting membrane, a position usually reserved
in other retinae for the cone nuclei (since cones ordinarily have plump
bases) ; the unusual plumpness of the amphibian red rod accounts for
the location of its nucleus.

Fig. 174 — Visual cells of anurans and urodeles. xlOOO.

a, single cone, double cone, red rod, and green rod of leopard frog, Rana pipiens (in other
families of anurans, the cones lack oil-droplets).

b, single cone, double cone, red rod, and green rod of tiger salamander, Ambystoma tigrinum.

The cones of ranid frogs possess oil-droplets, some at least of which
are yellow in life; and the double elements are built on the standard
plan (see Fig. 24a, b, c, p. 59). Bufonids and hylids, probably also other
nocturnal forms (e.g., pelobatids, brachycephalids,* microhylids, poly-

*Some of these however {e.g., Atelopus, Dendrobates) ate reported by the late G. K.
Noble (personal communication) to be strongly diurnal. Such anurans may prove to have
colored oil-droplets, or some substitute for them such as a yellow lens or cornea.

600 AMPHIBIANS

pedatids) differ from the arhythmic ranids in their total lack of oil-
droplets.

The anuran (and urodele) visual-cell patterns share features in com-
mon with the holostean and with the dipnoan (see Fig. 170b, p. 587;
Fig. 171, p. 591; and Plate I). The single and double cones of amphib-
ians and those of Amia and of Protopterus are clearly homologous,
respectively. It seems highly signficant however that the immature frog
(tadpole) rod has been claimed by several investigators to have an oil-
droplet, which it loses before or during metamorphosis. If this can be
confirmed, the implication is that the frog's rods were once single cones.
If their derivation was a recent one, then there may have been no rods
at all in the stegocephalians (which, we may be sure, were diurnal — see
pp. 164, 208, 274, 518-9). And, the cone-like characteristics of the
amphibians' peculiar 'green' rod (see p. 58) make this element in a sense
structurally, perhaps therefore genetically, intermediate between the
single cone and the ordinary or red rod (Plate I). It is possible how-
ever that the Stegocephali did have a rod type, homologous with that
of the Chondrostei and Protopterus, and that likewise it contained an
oil-droplet — which the frog, in its infancy, still remembers. The presence
of oil-droplets in the cones of both anuran amphibians and modem rep-
tiles is proof enough that the common ancestors (Stegocephali) had such
droplets — ^presumably, colored ones, else they would have gotten lost.

(B) Urodeles

The tailed amphibians compose eight families in five suborders. The
members of four of these families (Crytobranchidae, Amphiumidas, Pro-
teidae, Sirenidse) are 'larval' or 'partly metamorphosed' forms which are
permanently aquatic, and whose eyes are in a state of degeneracy or on
the ragged edge of it. Even among the other families — the primitive
Hynobiidae, their offshoots the Ambystomidae and their cousins the
Salamandridas, and the latter 's American derivatives the Plethodontidae
— there are scattered genera with greatly reduced or (cave-dwellers)
wholly degenerate eyes. At its very best, as in newts and especially in
terrestrial forms, the urodele eye is relatively small as compared with
the anuran, and its importance to the animal is relatively less. It is also
comparatively simple; but it cannot be too strongly emphasized that the
urodele pattern is not to be looked upon either as directly ancestral to
the anuran ocular plan, or as a descendant simplification thereof. The

THE URODELE EYE 601

resemblances between urodele and anuran eyes are by no means co-
incidental, but they represent only inheritances from a common ancestry
of great antiquity — probably, a single stegocephalian type. Otherwise,
some of the truly remarkable similarities would be hard to explain
inasmuch as it is certain that neither the urodeles were ancestral to the
anurans, nor rice versa.

The Eye as a Whole — Accompanying the usual oculorotatory muscles
is a retractor bulbi which, as in anurans, may be contracted not only to
protect the eyeball but also to use the latter as an aid to swallowing;
for, the partition between orbit and mouth cavity is purely membranous.
The lacrimal and Harderian glands are about equally prominent. Both
are distributed along the lower lid, and are sometimes not discriminable.
The lids form at metamorphosis if at all — they are lacking in the
permanently aquatic forms; and there is never more than a rudimentary
'nictitans'.

The eyeball is spherical excepting in some of the good-eyed aquatic
forms (e.g., Onychodactylus, some newts), in which the cornea is some-
what flattened in a fish-like manner. The cornea shows the same layers
as that of Rana, and likewise is completed at metamorphosis in those
salamanders which thereafter live on land. In the proteid Necturus, the
pAmary cornea also fuses with the skin; but since no sulcus then forms
around the eyeball, the latter is completely immobilized despite the pres-
ence of tiny extra-ocular muscles. This same situation perhaps obtains
in some of the other half -transformed, permanently aquatic salamanders.

The lens being relatively enormous in keeping with the generally
secretive habits of the group, the anterior chamber is shallow as com-
pared with that of an anuran. The sclera contains the expected hyaline
cartilage, but this is subject to great variations. In the Ambystomidae
it is a cup like that of the Anura, extending forward at least to the
equator and persisting throughout life. But in their presumptive ances-
tors, the Hynobiidae, the larval eye contains only a ring of cartilage (c/.
teleosts), and this becomes fragmented at metamorphosis. In the sala-
mandrids and plethodontids a larval ring disappears at metamorphosis,
only bits of cartilage remaining in some individuals of certain species
ie.g., Triturus pyrrhogdster) . In the monstrous cryptobranchid Megalo-
batrachus maximus, on the other hand, the scleral cartilage is disharmon-
iously hypertrophied to a degree unmatched elsewhere in the vertebrates
— in a horizontal section of the eyeball, two-thirds of its area is cartilage.

602 AMPHIBIANS

The cornea of this form is also abnormal in that it contains blood ves-
sels (but the ca. 9mm. eyeball could not properly be called degenerate) .
The closely related Cryptobranchus alleghaniensis also has an overgrown
scleral cartilage, equal in thickness to the radius of the lens. TTie con-
nective-tissue capsule of the minute and vestigial eye of the only Eu-
ropean cave salamander, Proteus, contains only bits of cartilage; and
the cartilage in the sole American proteid, Necturus, is also discontin-
uous. Cartilage is sometimes present in the permanently larval American
cave salamander Typhlomolge, but occurs in its relative, Typhlotriton,
only prior to the metamorphosis which this cave salamander, alone of all
such, experiences. In general, then, it may be said that whereas the
anurans lack scleral cartilage as larvae and possess it as adults, in the
urodeles this situation is reversed. It would be interesting to know
whether the tadpole of Pseudacris has scleral cartilage (see p. 595).

The chorioid is relatively thicker than in anurans, but more loosely
organized, with pigmented connective-tissue membranes running in quite
helter-skelter fashion. The circulation of the chorioid and iris is much
as in Rana, but the details have not been as well worked out for any
urodele. The ciliary body is triangular in meridional section and much
smaller than in anurans. There are no folds on the ciliary body or the
iris, excepting the single mid-ventral 'ciliary process' into which the
accommodatory muscle inserts. The iridic portion of this process is essen-
tially a seam formed by the closure of the embryonic fissure of the optic
cup — such a seam is quite generally present in lower vertebrates, run-
ning all the way to the pupil margin.* Urodeles have no canal (s) of
Schlemm; but crescentic ciliary muscles are present dorsally and ven-
trally in some forms (though not, apparently, in Ambystoma) .

There are no pupillary nodules, but otherwise the structure of the iris
is like that of the frog's. There is only a single, ventral, protractor
lentis muscle. This appears to be strictly comparable with its anuran
counterpart — and it will be recalled that an anuran can lack the dorsal
muscle. The lens is relatively larger and more nearly spherical (especially
in larvae and aquatic adults) than in the Anura (e.g., Necturus — equa-
torial diameter only 1.05 >; axial). It is most strongly supported by the
mid-dorsal fibers of the anuran-like zonule (cf. fishes), less well by
the mid-ventral ones, and depends least upon those in other sectors.

*It will be recalled that in mammals (see pp. 115-6) the blind part of the retina is not a
portion, but rather an outgrowth, of the optic cup; hence, it never normally contains a por-
tion of the embryonic fissure, which has healed before the commencement of the outgrowth.

THE URODELE RETINA 603

The Retina — The retina of a salamander differs from that of a frog
chiefly in the larger size and smaller number of its elements, and in the
total absence of vitreal or hyaloid vessels. The latter are presumably
dispensable owing to the smaller size of the eye and — probably — lower
metabolic rate of the retina (owing to the paucity of cones) . Large-eyed
forms tend to have thin retinae with extensive summation, the whole eye
being thus devoted to sensitivity. Small-eyed forms have thicker retinae,
in which no great pains have been taken to promote sensitivity through
summation or otherwise. But salamanders in general have much higher
visual-to-ganglion cell ratios than do the frogs. Whereas Rana pipiens
has about three visual cells per optic nerve fiber (within the area
centralis) , Burkhardt computed the following numbers of visual cells per
opticus fiber in American salamanders: Amby stoma maculatiim, 11;
A. jejfersonianum, 8; Triturus viridescens, 7; Eurycea bislineata, 22;
Desmognathus fuscus, 19; Plethodon glutinosus, 12; and Hemidactyl-
ium scutatum, 19.

The visual cells are of the same morphological types as those of anuran
amphibians (Fig, 174, p. 599). Both rods and cones are present in all
species excepting the four cave forms, whose visual cells are mere nub-
bins and all alike, reduced by degeneracy to a common denominator.
But not all salamanders have green rods (they are definitely stated by
European investigators to be lacking in Salamandra, though present in
Triton [-Triturus]) ; and cones — particularly the double ones — may be
sparse in strongly light-shunning forms {e.g., Megalobatrachus) . Both
the rods and the cones tend to be shorter and stouter than those of frogs
and toads, and indeed the red rod of Necttirus, two and a half times
the diameter of that of a frog, is the thickest known to science.*

The absence of cone oil-droplets is in adaptation to the habits of the
animals, as in non-ranid anurans, and does not prejudice against the
presence of colored oil-droplets in the ancestral Stegocephali (see Plate
I). In its own way, the urodele rod gives evidence of cone-ancestry:
though it does not have an oil-droplet when immature (cf. Rana) , it can
and does sometimes exhibit another cone-organelle, the paraboloid (e.g.,
in Necturus).

*It is for Necturus that the only counts of the retinal elements of an entire eye have ever
been made for any vertebrate. Palmer, in 1922, found about 53,000 rods, 42,000 single
cones, and 15,000 double cones in an average-sized retina, along with 176,000 inner-nuclear
elements (26,734 of these being Miiller fibers) and 30,464 ganglion-layer cell-bodies (most
of them glial — the optic nerve, near the chiasma, showed only 962 fibers).

604 AMPHIBIANS

Comparison with Fishes — We should naturally like to find, in the
eyes of the chondrostean— >dipnoan-^crossopterygian series of fishes,
the prototypes of all the distinctively amphibian features. This is not
possible; and we may never have the story much more complete, even if
Latimeria is retaken and is studied by the right people. The eye of, say,
Amby stoma tigrinum compares quite strikingly with that of Protopterus;
but many of the similarities are matters of anatomy and of optics, and
our attention here should be strictly on the morphology. Again, it is
certain that the Protopterus eye has been secondarily simplified, and it
is very likely indeed that the most complex of modern urodele eyes lack
many features which the first urodeles possessed. Could we but restore
the lost details to both Protopterus and Ambystoma, we might still find
amazing similarity — or we might be unpleasantly surprised. When two
structures, complex in two different ways, are simplified secondarily they
may become closely identical without this having the least phylogenetic
significance. Witness the similarity of the eye of Protopterus to that of
a brook lamprey, no more closely related than an owl is to a gecko.

Such things as the amphibian tadpole's spectacle, and its spherical
lens, are lungfish-like only because the tadpole is aquatic. The fact that
the Protopterus lens lies behind the iris means only that the eye is dis-
harmonious, not that it is pre-adapted for aerial vision. Some other parts
of the Protopterus eye — the chorioid, for example — are too much re-
duced to afford any comparisons. Neither lungfishes nor amphibians
have an annular ligament, which developed in the chondrosteans and
went on up the holostean-^teleost branch of the piscine tree; but this
is a negative sort of resemblance — as well say that neither group has a
chorioid gland; and, we have seen (brook lampreys!) that the structure
can be absent in forms whose better-eyed relatives have it. Either ancient
lungfishes, ancient amphibians, or both may have had annular ligaments
as well as a number of other things.

Many amphibian features are entirely 'new', and while some of them
may serve to link the group with higher forms, none can have any
significance for the derivation of the amphibian ocular pattern from
anything below. Among such features must certainly be listed the re-
tractor and levator bulbi muscles, the extra-ocular glands, the lids, the
iris folds (homoiologous, only, with those of elasmobranchs) and pupil-
lary nodules of anurans, the loss of the argentea, the secondarv absence
of scleral cartilage in some adults and its delayed formation in urodeles,
the protractor muscles (at least the dorsal one of anurans) , the fibrous

COMPARISON WITH FISHES; CJECILIANS 605

zonule, the (secondary) absence of oil-droplets in most species, and the
green rods of the retina. The 'canals of Schlemm' of anurans are prob-
ably unique, and the ciliary muscles are surely not the same thing as the
teleostean 'tensor chorioideae'.

But the amphibian eye is of course not wholly new. Though its iris
muscles, like those of elasmobranchs (and teleosts), represent independ-
ent inventions, their beginnings are perhaps seen in the contractility of
the unmodified iris epithelium of Protopterus. The mid- ventral 'ciliary
process' may have been inherited ultimately from the similar structure
in the chondrosteans, and may thus be a distant cousin of the campanula
Halleri. A strong point is the identical course of blood supply to the
vitreal vessels in anurans, Protopterus, and Polypterus (shared also with
Amia and with the catfishes among the teleosts). The urodeles probably
lack such vessels only through secondary loss. Most striking of all is the
resemblance of the visual-cell patterns of Protopterus and the amphib-
ians, emphasized diagrammatically in Plate I. When one considers how-
ever that the visual cells are phylogenetically the oldest and most funda-
mental elements in the whole eye, it should perhaps not be surprising
that in the present instance they seem especially reliable illuminants of
the dim pathway of phylogeny.

(C) C^CILIANS

The Caecilia or Gymnophiona are legless, worm-like amphibians which
are restricted to the tropics. The single, homogeneous family contains
55 species in nineteen genera. All, except the aquatic Typhlonectes,
spend most of their time underground. Their eyes are very small, but
have well-developed retinae and are useful for the registration of light-
intensities and directions. The most important sense-organ is the unique
retractile tentacle, which has both tactual and olfactory capacities. Sev-
eral adjuncts of the eye have been commandeered by this more useful
organ. The eyes of the Ceylonese Ichthyophis glutinosus and of Hypo-
geophis alternans, a resident of the Seychelles, have been the most com-
pletely investigated.

The orbit is capacious, but is largely filled by the Harderian gland,
here serving to lubricate the sensory tentacle instead of the eye.* The
eyeball is two-thirds of a millimeter in diameter in a large Ichthyophis,

*This is not the only instance in which the Harderian has ceased to serve the eye primarily,
and has taken on a new funaion (see pp. 424, 455, and 635).

606 AMPHIBIANS

only 0.3mm. in Hypogeophis. The rotatory muscles are present in both
genera (lacking in Ccecilia and Herpele), though thin and largely ten-
dinous, and incapable of moving the eye owing to its attachment to the
overlying skin. In the larva, a retractor bulbi is properly attached to the
globe, but in later development it is seduced away by the tentacle to
become its retractor. The internal rectus serves to retract the tentacle
sheath, and a former levator bulbi is pressed into service as a compressor
muscle of the tentacular (Harderian) gland.

The eyeball lies beneath a transparent patch of skin, from which it
is separate only in the larva. In Hypogeophis, the primary cornea, a
continuation of the fibrous sclera, can still be identified after fusion with
the skin in the adult; but in the adult Ichthyophis the sclera appears to
intersect the corium of the skin, and the lens to contact the latter directly.
The chorioid is very thin, and is pigmented in Ichthyophis but not in
Hypogeophis. There is no ciliary body or any mechanism of accommo-
dation, and the iris consists entirely of the two epithelial retinal layers,
only the anterior of which is pigmented. The pupil is the same size as
the lens, which projects half-way through the aperture. The relatively
large lens is solid, somewhat flattened, and is cloudy in life (in Hypo-
geophis, at least) . Running through the small vitreous cavity from retina
to lens, in the position of a canal of Cloquet, is a strand of (meso-
dermal?) tissue.

The retina is quite respectable. There are no vitreal vessels. The pig-
ment epithelium bears many fine, pigmented processes, in which there
is no pigment migration. Only massive rods, simple in structure (no
oil-droplets or paraboloids) are present. In Hypogeophis the outer nu-
clear layer has two to three rows of nuclei, the inner nuclear three, and
the ganglion layer two. Corresponding figures for Ichthyophis are: 2,
2-3, 1. In the latter genus the optic papilla is triple, the three branches
of the optic nerve lying in one vertical plane icf. Polypterus) . No optic
chiasma is visible outside the brain.

Chapter 16
REPTILES

See also pages: 251 Figs, 99, 100

58-9 visual cells 257,269-83,417 accommodation, refraction

118-9 embryology 293-6 visual fields

134-9 origin, relationships 305-7 eye movements

150 photomechanical changes 339 Fig. 124c, parietal eye

164-5, 205, 208 habits 365 pecten (conus)

187, 306-7 area centralis, fovea 419, 450-9 adnexa

210 fossorial forms 494-7, 518-20 color vision

240-1 tapeta, eyeshine 538-43 dermal color changes

The eyes of the various types of reptiles are much alike except for the
snakes, which are set sharply off from all the others. The class as a whole
exhibits a number of features whose origins cannot be traced by any
scrutiny of living amphibians. If a good fairy should offer the compar-
ative ophthalmologist a living specimen of any one archaic vertebrate,
his choice should certainly be Seymouria, that stegocephalian which was
the 'first reptile'. Lacking such a miraculous resurrection, we are no
better able to link the exclusive features of the reptilian ocular pattern
to the elements of the amphibian plan, than we were to see the origins of
the lissamphibian features in any of the so-far-studied lunged fishes.

The reptiles perfected the terrestrially-adaptive accessory organs which
the amphibians had been forced to invent, and also made the most of
their opportunity to develop a powerful, lens-squeezing mechanism of
accommodation (see pp. 417-23, 592-3). Their most characteristic intra-
ocular features are all means to this latter end : the striated ciliary muscle
fixed (usually) to the rim of the cornea, the scleral ossicles and the con-
cavity which they support, the 'ringwulst' or annular pad of the lens, and
the tall ciliary processes which are fused to the lens capsule and are in
all probability genetically independent of the uveal folds of modern
tailless amphibians. Along with these structures, the reptiles have pro-
duced a striated (though ectodermal) iris musculature and a pigmented,
richly vascularized, conical protrusion from the optic nerve head (the
'conus papillaris'), whose framework is ectodermal (neuroglial) and
whose function is to nourish the inner layers of the retina (in lieu of
vitreal or intrinsic retinal vessels) by diffusion through the vitreous, after

607

608 REPTILES

the fashion of the teleostean falciform process. Of all the reptilian
peculiarities, only the transversalis muscle may be homologous with any-
thing in the living amphibians (i.e., with their ventral protractor lentis).
The early reptiles adopted strict diurnality and a pure-cone retina; but
many of the living forms and sub-groups have backslid into nocturnality,
supporting this habit with a rod-rich or even pure-rod retina whose rods
are transmuted cones in every case.

To every one of the above statements the snakes constitute a conspic-
uous exception. There is nothing whatever 'reptilian' about their eyes,
which exhibit instead a number of features which are uniquely ophidian.
Indeed, the snake eye is such a conglomeration of 'Ersatz' that it might
well be imagined to have come from another world. Zoologists have long
been fond of citing the cephalopod molluscs, as showing how nearly an
invertebrate group can imitate the vertebrate eye if it tries hard (see Fig.
Ig, p. 3). They might give at least as much credit to the snakes; for in
them, we see a vertebrate group which has been under the necessity of du-
plicating the vertebrate eye, and has made a very good job of it. This no
doubt obscure statement will be clarified by the discussion in Section D.

(A) Chelonians

See also pages:

59 Fig. 24c 251 Fig. 100

72 vision 272-9, 436-8 accommodation, refraaion

101-2 zapfensubstanz 274 scleral ossicles

135, 138 Fig. 60, relationships 293 visual fields

177 retina ^^^ eye movements

184,187,190,305 area centralis, fovea ,^^ parieta eye

344 movement-perception
^^^ ^'S-^^ 422-3,428,450,457-8 adnexa

191-8,202 oiWroplets 435^ amphibious adaptations

216 visual cells 494.6, 519 color vision

224 pupil 546-7 coloration of eye

Though obviously highly specialized, the Chelonia are nevertheless
the most archaic of the living orders of reptiles — closest of all to the stem
group, the Cotylosauria. They are cosmopolitan, and comprise eleven
families in four suborders. The taxonomic differentiation of the group
is of less importance to us here than the ecological — into the strictly
aquatic marine 'turtles' (s.s.), the amphibious, freshwater 'terrapins', and
the strictly terrestrial 'tortoises' (see, especially, the references to accom-
modation and adnexa) .

THE CHELONIAN EYE

609

The Eye as a Whole — The eyeball has equal vertical and horizontal
diameters, and a slightly shorter axial diameter (Fig. 175). Its internal
proportions are those of a diurnal eye with a broad retinal image and
high resolution. At the same time, its dioptric media are the most trans-
parent known — which one would expect to be true of some nocturnal
animal.

The sclera consists largely of a cup of cartilage which reaches forward
beyond the equator, from where the zone occupied by the scleral ossicles
extends to the corneal rim as a flat-surfaced, truncated cone. The cornea
is thick (except in sea turtles?) and bears a relatively thick epithelium
and prominent Descemet's layers. The substantia propria, at the limbus,
divides into two portions, the inner of which receives the tendinous

Fig. 175 — Right eye of a turtle,
Testudo graca, in horizontal section.
Redrawn, modified, from Szent-
Gyorgyi. (The lens is shown in full
accommodation ) .

c- chorioid; co- conjunctiva; cs- canal
of Schlemm; he- hyaloid canal of
vitreous; /- lens; mt- meshwork tissue
of iris angle; n- nasal side; o- optic
nerve; r- retina; sc- scleral cartilage;
so- scleral ossicles; t- temporal side;
Z- zonule.

origins of the ciliary-muscle fibers, while the outer splits to enclose the
scleral ossicles and then recombines to pass over the outer surface of the
scleral cartilage as the fibrous layer of the sclera. As in reptiles in gen-
eral, the boundary between cornea and sclera is indicated by a deposit
of pigment in the fibrous tunic.

The chorioid is of ordinary thickness and is not richly vascular except
in marine forms. Anteriorly, where the chorioid merges into the ciliary
body, the inner layers of the uveal coat, together with their epithelial
(retinal) facing, swing gradually away from the fibrous tunic, leaving a
long, sharp cleft to be filled in with loose connective tissue which thus
suspends the iris from the limbus corneae. The canal of Schlemm lies
against the sclera in this meshwork tissue, in a position approximating

610 REPTILES

closely that of the amphibian canals (see Fig. 173, p. 595). This early
divergence (i.e., as one passes forward from behind) of the uvea and
sclera — characteristic also of other reptiles and of birds (see Figs. 109,
112; pp. 275, 280) — helps to approximate the ciliary body to the pe-
riphery of the lens. The 40-60 ciliary processes (Fig. 110, p. 277) have
their crests firmly fused to the lens capsule (except in some or all marine
forms) . They send continuations a little way onto the iris.

The ciliary muscle fibers are mostly meridional in orientation. They
originate from the inner layers of the substantia propria of the cornea
and run close to the sclera to terminate in the connective tissue of the
flat posterior zone (orbiculus) of the ciliary body. The muscle as a whole
is small in land forms and terrapins, in which the sphincter iridis does
most of the work of accommodation. But in marine turtles, which have
not much needed to employ the iris muscle for deforming the lens (since
they are limited to aquatic vision, and need no tremendous range of
accommodation), the ciliary muscle is massive; and this is probably a
primitive situation. The transversalis muscle (see pp. 269, 279, 299)
originates in the connective tissue between the ciliary body and sclera,
ventrally, and passes through a portion of the (otherwise healed) em-
bryonic fissure of the pars caeca retinae to pull on a group of zonule fibers
which serve as its tendon. Its relationships are thus much like those of
the amphibian's ventral protractor lentis, with which it is conceivably
homologous.

The iris is not sharply demarcated from the ciliary body, since the
base-plate of the latter is largely separated from the sclera and makes
no sharp angle with the iris at the latter 's periphery. Both retinal layers
are pigmented, and it is doubtful whether the anterior layer ever gives
rise to a dilatator comparable with that of the mammals. Radial muscle
fibers may be seen even contiguous with the anterior retinal layer, but
these are nucleated and are probably only re-oriented derivatives of the
massive sphincter muscle, which occupies the whole breadth of the iris
from pupil to root.

The lens is the softest, most pliable in the vertebrates. It is flattest in
the tortoises (equatorial-axial diametral ratio 1.6 in Testudo grceca) ,
less flat ica. 1.3) in terrapins, and virtually spherical in sea-turtles —
where of course it need not be prepared to deform as much as in the
other types of chelonians, but needs a strong curvature when at rest
owing to the optical absence of the cornea. The 'ringwulst' is weakly
developed in chelonians. The primary vitreous of the embryo is not

THE CHELONIAN RETINA 611

represented (as in fishes, amphibians, and other reptiles) by a broad
funnel whose mouth coincides roughly with the retinal ora terminalis.
Instead, there is a slender canal of fairly uniform diameter which runs
forward from the disc, like the mammalian canal of Cloquet, but does
not reach and touch the lens; rather, it ends on the anterior hyaloid
membrane toward the temporal side (Fig, 175).

The vascular pattern of the eyeball, as worked out by Fritzberg on
Emys orbicularis, compares quite closely with that of the frog. There are
no vitreal vessels, however — their place was probably taken (physiolog-
ically) in primitive reptiles by the conus papillaris (p. 607) ; but no
well-developed conus occurs in any known adult chelonian. In advanced
embryos of Chelonia, Chrysemys, and Chelydra, a small, unpigmented,
avascular glial cone forms upon the nerve head; but in the adults of
these genera (except perhaps Chelonia) , the surface of the 'disc' smooth-
ly continues that of the surrounding retina. It is difficult to say why the
turtles have been able to dispense with (or to avoid evolving?) a conus
when the lizards have not, for the turtle retina is nearly as rich in cones;
but the general difference in activity of turtles and lizards is perhaps
the explanation (see p. 653). The poor development of the average
chelonian chorioid strongly suggests that the metabolic requirements of
the retina are relatively low.

The Retina — The retina is decidedly impure in its lamination (Fig.
176a), with every nuclear layer containing some elements which 'belong'
at some other level. The horizontal cells have ropy processes, and may
have reverted completely to a non-conductive function. All or nearly all
chelonians have an area centralis. Outside of this, the visual: ganglion
cell ratio is in the neighborhood of 2:1; but within the area there is of
course a lower summation-ratio. A fovea has been claimed, and later
authoritatively denied, for each of several genera; but such a feature has
been convincingly demonstrated (by photomicrography) only in Amyda
(by Gillett, who failed to realize the uniqueness of his discovery) .

Prior to 1877, about everyone who described a chelonian retina saw
rods in it, but since that time, owing to one of the few mistakes (and
the weighty authority) of Max Schultze, the turtles have been placed
among the pure-cone reptiles. They do however possess droplet-free ele-
ments with heavy, cylindrical outer segments, morphologically identical
with the unquestionable (rhodopsin-containing) rods of crocodilians
and with the plump peripheral rods of birds. It is not known whether
these cells contain rhodopsin, but since they are most numerous in the

REPTILES

light-shunning turtles it is clear that they are physiologically rods, bear-
ing several signs of cone ancestry (Fig. 176b and Plate I).

Rods are perhaps lacking in the foveate Amy da (Gillett figures only
cones), but this form's suborder, the Trionychoidea, is not primitive,
though characterized by a soft shell (so, secondarily) , We may be sure
that these droplet-free elements, serving originally as cones, were part of
the cotylosaurs' equipment, though their origin (presumably from drop-
let-bearing cones) cannot be traced
in any living vertebrates (Plate I) .
The other visual-cell types of the
turtle group are the same droplet-
bearing single and double cones
which we have already seen in the
amphibians and traced to the ar-
chaic Chondrostei (Fig. 176b; cj.
Fig. 174a, p. 599).

g#;

^ @

Fig. 176 — The chelonian retina and its visual cells.

a, retina of common snapping turtle, Chelydra serpentina. x500.

a- amacrine cells; d- double cone; g- ganglion cell; h- horizontal cells (ropy type); 'm-
Miiller fiber; n- bundle of nerve fibers; o- outer nuclear layer; p- pigment epithelium;
r- rod; s- single cone.

b, single cone, double cone, and rod of Chelydra serpentina, x 1000.

THE CROCODILIAN EYE 613

(B) Crocodilians

See also pages:

270, 274 sclera, ossicles

135, 138 relationships

272-9, 436 accommodation, refraaion

145, 543 habits

293 visual fields

162, 224, 501 pupil

305 eye movements

184 area centralis

436 amphibious adaptations

202-3 oil-droplets

496 vision, color vision

207 visual acuity

519 Fig. 156

231,238,240 tapetum,

eyeshine

542-3 dermal color changes

251 Fig. 100

544 coloration of eye

The Eye as a Whole — In this small group of large reptiles the eyeball
bears the stigmata of a long-continued noctumality, which has affected
every part of the organ. The specializations of the adnexa are directed
toward the largely aquatic activities of the group (see pp. 421-2). The
globe is of 'nocturnal' size, its diameter reaching 20nim. in the alligator
and exceeding this value in larger types. The eye of the American alli-
gator (Alligator mississippiensis) is better known than that of any other
form; but nearly all the studies of it have been made by European
investigators.

The sclera has retained the ancestral cartilaginous cup, but has lost
the annulus of ossicles. Their disappearance has permitted the circum-
corneal zone of the sclera to become convexly curved like the rest of the
fibrous tunic. The eyeball is consequently practically a sphere, though
a bit shortened axially. The cartilage reaches nearly to the ora terminalis,
which lies a little in front of the equator. The purely fibrous tissue
anterior to the cartilage is greatly thickened, but thins again before it
coalesces with the substantia propria of the thin cornea.

The chorioid is thick and richly vascular behind the tapetum iv.i.),
thin and poor in vessels elsewhere. The broad ciliary body shows — even
more markedly — the same divergence of the base-plate (bearing the
ciliary processes) from the muscular lamina (clinging to the sclera)
which we noted in the turtles. The cleft thus formed at the periphery of
the anterior chamber is filled by a wedge-shaped (in section) mass of
loose connective tissue, the anteriormost strands of which run directly
from the cornea to the root of the iris to form a pectinate ligament.*
The much-branched canal of Schlemm does not, as in turtles, lie in this
meshwork tissue, but is completely embedded in the thick contiguous
sclera.

''For an analogous situation, see Figure 191, p. 645,

614 REPTILES

The loss of the scleral ossicles in these animals is coupled with a
virtual disappearance of the ringwulst of the lens. These two losses are
clearly related to the noctumality of the crocodilians and their conse-
quent lack of need of much or any accommodatory capacity. The evolu-
tionary outbulging of the circumcomeal sclera upon the loss of its sup-
porting bones, and the inward shrinkage of the lens equator owing to
the thinning of the annular pad, have not however taken the ciliary body
entirely out of contact with the lens (as these same changes have done in
the mammals) . In the crocodilians the hundred-or-more greatly elongated
ciliary processes — they have been called 'tongue-like' — still contact the
thick capsule of the lens at its equator; and according to Beer and Hess
the accommodatory effort, though slight and exerted with extreme slow-
ness, is still sufficient to pull inward the circumcomeal zone of the sclera
and produce some bulging of the center of the rather flat anterior surface
of the lens.* The (wholly meridional?) ciliary muscle lies in the sclerad
lamina of the ciliary body, and is scarcely as well developed as in terra-
pins. Its fibers underlie the orbiculus, far distant from the limbus, with
their anterior ends attached to the inner surface of the scleral thickening
and their posterior insertions in the meshwork tissue close to the anterior
border of the chorioid.

The accommodatory equipment centering around the ciliary muscle is
thus at a low ebb in the crocodilians, as in the turtles — but not for the
same reason: in the former, it is a logical consequence of an age-old
noctumaUty with its crude images and its indifference toward a precise
focusing thereof, while in the turtles it is owing to the fact that the
pupillary sphincter has taken on most of the work of increasing the curv-
atures and focusing power of the lens. The transversalis muscle, if ever
present in early crocodilians, is apparently lacking in living species.

The deep pigmentation of the thick iris stroma is concealed in the
living animal by an anteriormost layer of lipophores which gives the
iris a lemon or cream color. The sphincter resembles that of turtles in
that its fibers are distributed throughout the whole width of the iris,
though concentrated only near the pupil. The posterior retinal layer is
heavily pigmented and cuboidal. The anterior is squamous and unpig-
mented. It may be radially contractile; but it is generally denied that a
dilatator is ever present in crocodilians — which may largely explain why
the alligator's pupil is so slow to open (p. 501).

*The periphery of which surface only flattens the more during accommodation, being pre-
sumably kept from sharing in the 'bulge' by the pressure of the iris against it.

THE CROCODILIAN RETINA

615

The Retina — The crocodilian retina is strongly 'nocturnal' in organ-
ization, and seems to have long ago lost any need for nutritive provisions
other than the chorioid. At any rate, the only traces of a former conus
papillaris (if indeed they are such remnants!) are a glial pad on the
adult disc, which contains a capillary or two but scarcely protrudes
toward the vitreous at all, and a superficial dusting thereof with melanin
granules. The following remarks apply to the alligator:

The pigment epithelium is highly modified, in the superior half of the
retinal cup, forming a guanin tapetum lucidum (q.v.). Toward the

Fig. 177 — Representative visual cells of a crocodilian, Alligator mississippiensis. xlOOO.

a, single cone, double cone, and rod (the cones from the ventral fundus; the rod frotn the
region of the tapetum lucidum).

b, single and double, partially-transmuted cones from opposite the center of the taf>etum.

ventral border of the tapetalized area there is a horizontally-elongate
area centralis, from which no attempt seems to have been made to elim-
inate the rods, though all the visual cells have here been slenderized
and aggregated.

The horizontal cells are not quite as heavy-fibered as those of turtles;
but the Miiller fibers are particularly numerous and conspicuous. The
extent of summation may be gathered from the fact that there are one
to one and a half rows of outer nuclei, four to five rows of inner ones,
and a single scattered row of ganglion-cell nuclei.

616 REPTILES

The types of visual cells (Fig. 177a) are the same three as in the
turtles (c/. Fig. 176b, p. 612), and are respectively homologous with
them (see Plate I). The oil-droplets have long since been discarded
from the cones, however,* and the rods are rich in rhodopsin and greatly
outnumber the cones, instead of constituting a minority of the visual
cells as in even the most photophobic of chelonians.

In the region backed up by the tapetum, it might be expected that the
cones would have become diminished in numbers or even eliminated,
to make that much more room for sensitive rods. Instead, the cones have
been retained; but their outer segments — even in the 'area centralis' —
have been made as rod-like as possible {i.e., heavy and cylindrical — Fig.
177b). Within this single retina we may thus observe a local, partial
transmutation of cones into rods. These 'intermediate' visual cells are
interestingly like the droplet-bearing elements of Sphenodon (Fig. 179,
p. 621) in their morphology — and no doubt, to a degree, in their
physiology.

(C) Sphenodon

See also pages: 216 visual cells

78 rhodopsin 224 pupil

135, 138 relationships 251 Fig. 100

189-90 Fig. 82, visual cells, fovea 274 scleral ossicles

200-2 oil-droplets 339-40 parietal eye

206 vision 497, 519-20 color vision

This single living member of the Rhynchocephalia was originally
thought to be a lizard, and was placed in the lacertilian family Agamidae.
Its true nature transpired at a time when the rhynchocephalians were
supposed to be very primitive. Anatomically, Sphenodon is indeed
'generalized' as compared with the highly specialized — though far older
— chelonians and crocodilians. But its position in modern taxonomy is
near the lizards.

All sorts of efforts have been made to see the Sphenodon eye as the
'most primitive' sauropsidan optic; but it is nothing of the kind. So far
as the eye is concerned, Sphenodon can best be described as a pre-lizard
which has gone off the beaten track into nocturnality.

*In Alligator and perhaps in all; but mentions of colorless oil-droplets (in unnamed
species!) occur in even recent literature.

THE EYE OF SPHENODON 617

The Eye as a Whole — The adnexa bear closer resemblance to those of
lizards than to those of amphibians or other reptiles (see pp. 420-3, Fig.
143 on p. 421), The lacrimal gland can be lacking in a lizard (as it is in
Sphenodon). The nictitans tendon attaches to the orbital wall in Sphen-
odon as in lizards; and the nictitans musculatures are mutually convert-
ible. The two-headed retractor bulbi of Sphenodon is the largest of the
extra-ocular muscles, and is innervated not only by a branch of the sixth
cranial (abducens) nerve but also by a sprig from the ciliary ganglion.

The eyeball has been described in its entirety only by Osawa (1898),
who made certain errors and oversights. It is large for the size of the
animal (as compared with a diurnal lizard) , with an equatorial diameter
of 17mm. and a slightly shorter axis. A considerable change in surface
curvature takes place at the limbus, creating a sclero-corneal sulcus
(which, it will be remembered, we have not seen in any forms below
Sphenodon, but which we will encounter regularly hereafter).

The sclera contains a cartilaginous cup, and, including the fibrous
layer outside of this, is about as thick as the retina. Anteriorly the carti-
lage extends about to the ora terminalis, and is there overlapped slightly
(externally) by the circlet of scleral ossicles.* These agree in number
(16-17) better with those of lizards (12-15) than with those of turtles
(6-11). The cornea is strongly arched, of uniform thickness throughout,
and is 9.5mm. in diameter — the same size as that of an Iguana eye of the
same diameter, but relatively large as compared with that of such a sun-
worshipping diurnal lizard as the deserticolous Uromastix (eye 12mm.,
cornea 3.4). The cornea has a thin epithelium (consisting of only two
layers of cuboidal cells with round nuclei) , Descemet layers, and a thick
propria which contains no such vertical fibers as are described by Osawa.
The inner layers of its fibers, at the margin of the cornea, blend into a
narrow thickened zone of the sclera which lies opposite the iris root.

The chorioid is especially heavily pigmented on its scleral side. It is
thicker than in small-eyed lizards (but no thicker than in, say, Varanus) ,
and is well vascularized. Grouped and scattered in it are peculiar spher-
oidal pigment cells with central nuclei suspended by delicate protoplas-
mic strands, as in a brown-fat cell. These cells form a dense aggregation
opposite the fovea (not visible, owing to bleaching, in Fig. 82 on p. 189).
The glass membrane can be easily followed through the ciliary body
(where it is greatly thickened), but not into the iris; and the chorio-
capillaris also extends well into the ciliary region.

*Not obvious (e.g., Fig. 178) unless section passes through center of ossicle.

618

REPTILES

The ciliary body increases gradually in thickness from behind for-
wards, from near-equality with the chorioid to about twice this value.
Its base-plate and epithelium do not, however, diverge widely from the
sclera, so that only a small amount of spongy tissue lies between (Fig.
178; contrast Fig. 191, p. 645). Osawa to the contrary, there are no
ciliary folds or processes — the inner surface of the broad ciliary body is
perfectly smooth, which seems an important point in agreement with the
lizards. Where the ciliary body joins the iris, there is a sharp 'corner' or

The anterior segment of Sphenodon punctatum. x 12.
cm- ciliary muscle (anterior, circumferential fibers show as
a group of dots beneath the canal of Schlemm); co- con-
junctiva; cs- canal of Schlemm (containing nerve, shown in
black); /- lens; ot- ora terminalis; r- ringwulst; sc- scleral
cartilage; so- scleral ossicles; i- zonule.

annular ridge, from the crest of which a delicate, elastic, radially fibrous
cuticular membrane — actually, the anteriormost 'leaf of the zonule —
passes straight to the posterior surface of the iris which it intersects at
about one-third of the way from iris root to pupil. Here it is as firmly
fused with the iris as with the lens capsule; and, if the lens and iris are
separated (in preserved eyes, at least), it remains attached to the iris
rather than to the lens. The zone of the iris thus bridged by this mem-
brane has a rugose posterior surface on which the low, undulant folds

THE EYE OF SPHENODON 619

run roughly radially; but these could hardly be called iris folds (e.g., in
the anuran sense).

The bridge-membrane, besides contributing to the anchorage of the
lens, probably helps to hold the iris against the periphery of the anterior
surface of the lens during accommodation — if any — by using the iris as
a third-class lever, thus confining the accommodatory deformation of the
lens surface to the portion behind the pupil (see footnote, p. 614).

Gross dissection reveals what is apparently a transversalis muscle; but
this lacks histological confirmation as yet.

In the loose meshwork of the ciliary body, the most conspicuous struc-
ture is the enormous canal of Schlemm, which lies at the inner side of
the sclera just behind the thickening at the iris root. Toward its posterior
side there is a large annular nerve, as in most lizards. The canal is sup-
posed to be lacking in Sphenodon (but Osawa was looking for it in the
sclera, where it seldom lies in reptiles; and his drawing shows it plainly
— unlabelled — in its true location) . The ciliary muscle is relatively weak.
It does not commence at the anterior end of the ciliary zone, but about
a quarter of the way back. Its fibers originate partly upon scleral tissue
lying behind the iris-root thickening, partly from the inner surface of the
sclera paralleling the posterior half of the ciliary body, and insert into
the connective tissue of the orbicular base-plate and on the outer surface
of the glass membrane in that region, a very few of them all the way
back to the ora terminalis. In horizontal sections of the eye, the anterior-
most ciliary-muscle fibers on one side of the eye are seen to be cut in
cross-section (c/. such lizards as Seps and Lacerta; p. 624).

According to Ida Mann the iris is covered anteriorly by a layer of
chocolate chromatophores, through breaks in which some coppery and
silvery-buff patches of deep-lying iridocytes can be seen in the living
animal. The blood vessels form a system of arcades aimed inward toward
the pupil, and many of them form loops which burst free of the iris
surface into the anterior chamber. This iridic circulatory pattern re-
sembles those of crocodilians and geckoes about equally well.* Muscle
fibers with a sphinctral function are evenly distributed throughout the
stroma from pupil to iris root; but they are concentrated toward the
periphery since the iris is thickest here and thins gradually toward the
pupil. The dilatator fibers lie against the epithelial retinal layers. It is
clear that they are direct derivatives of the sphincter (as perhaps in all

* Unfortunately, the vascular pattern of the whole eye of Sphenodon has never heen worked
out.

620 REPTILES

reptiles) , and TxOt parts of the underlying anterior-epithelial cells as are
the dilatator elements of mammals. Both retinal layers (as in lizards)
are heavily pigmented — the anterior, even more so than the posterior
(as in all vertebrates in which a dilatator is lacking or, if present, is not
formed as a lamina of the anterior retinal layer) .

The anterior chamber is very shallow and the lens is large — 8.0mm.
X 6.33mm. — in keeping with the nocturnal habits of the animal. Thus,
the quotient of eye diameter and lens diameter (17/8) is 2.12 in Spheno-
don, 2.7 in Iguana, and 2.78 in Uromastix icf. corneal proportions,
above). The flatness-index of the lens (8/6.33) is 1.26, while the lenses
of diurnal lizards average somewhat flatter (1.4-1.5) and that of a
terrestrial turtle (Testudo grceca) is flatter still (1.6). The alligator
lens is about as rotund as that of Sphenodon, however (1.25), and
nocturnal lizards (geckoes) have nearly spherical lenses (e.g., Tarentola
mauretanica — l.l). The Sphenodon eye may perhaps have a relatively
large retinal image for a nocturnal animal; but this is not out of line
with its retention of other features having to do with the maintenance
of good resolution — the fovea, for instance, as well as some of the saur-
opsidan adjuncts to good accommodation (scleral ossicles, ringwulst).
The anterior surface of the lens is much less sharply curved than the
posterior, and the ringwulst is well developed, its thickness being 6%
of the diameter of the whole lens.

There are no vitreal vessels; and there is no conus papillaris — and
even less trace of one than in the crocodilians, for the optic disc is not
even convex, and shows only a very few melanin granules. The disc is
slightly temporal and considerably ventral in position, its center lying
about 2.5mm. from that of the exactly (?) central fovea. The sensory
retina, as in large lizard eyes, tapers gradually in thickness anteriorly,
so that the ora is not abrupt. The optic nerve is relatively slender, with
a simple circular cross-section, and entirely lacks any septal system. Else-
where in the reptiles, so simple a situation occurs only in the (also
nocturnal) crocodilians.

The Retina — Because of the coarseness of its visual-cell mosaic and
its Miiller fibers (which become massive in the far periphery, and occupy
most of the volume of the retina there), the Sphenodon retina appears
at first glance to resemble that of the turtles. Closer analysis shows that
the strongest similarities are to the lizards. Sphenodon has a concavi-
clivate fovea (Fig. 82, p. 189), which in the diurnal ancestor was prob-
ably entirely lizard-like.

THE RETINA OF SPHENODON

621

The visual cells (Fig. 179; cf. Figs. 176b, 177a, 181; pp. 612, 615,
626) clearly explain the persistence of the fovea, which has been lost in
other nocturnal reptiles whose diurnal relatives are foveate (e.g., geckoes,
xantusiids, pygopodids). The matching single and double elements are
about equal in numbers and greatly predominant. They are manifestly
homologous with the single and double cone? of turtles and crocodilians;
but Sphenodon has converted them into physiological rods by enlarging
their outer segments and largely bleaching their oil-droplets — which,
however, have been retained (contrast Fig. 177b, p. 615).

The third, tiny type of element is very
scanty. Never more than twenty can be
counted in a 10 [I sagittal section of the large
(17mm.) eye. It is an unmodified droplet-
free cone, obviously useless to the animal
and on its way to total disappearance. By
reference to Plate I, it will be seen that this
element must be the same cotylosaurian-
eosuchian droplet-free cone which has be-
come a rod in the turtles and, independently,
in crocodilians (and still once more in the
birds or in their dinosaurian ancestors — see
p. 661). It seems thus to be a little-cone-
which-makes-a-better-rod. Why, in converting
over to nocturnality, Sphenodon elected in-
stead the two droplet-bearing elements for
transmutation into rods, cannot be explained.
But the droplet-free element has obviously
proven unsatisfactory in modern reptiles as
a cone — not only to Sphenodon, where it is
even excluded from the fovea — ordinarily a pure-cone region in other
vertebrates (not one shows in the field of the photograph in Fig. 82,
p. 189) — but also in the lizards, which eliminated it entirely (see Fig.
180a, p. 626).

Sphenodon very probably owes its long survival as a 'living fossil' to
its adoption of nocturnality, which was facilitated by the transmutation
of diurnal-ancestral cones into low-threshold elements, and expresses
itself elsewhere in the eye in the simplified optic nerve, the slit pupil, the
shallowed fovea, the enlarged lens (and cornea), the loss of the conus
papillaris (see p. 653), and the reduced accommodatory apparatus.

Fig. 179 — Representative visual

cells of Sphenodon punctatum:

single rod, double rod, and cone.

X 1000.

622 REPTILES

(D) Squamates

See also pages: 251 Figs. 99, 100

56, 61-3, 161-2, 165-8, 176, 178, 216, 254 254, 270, 272-3, 279-83, 438, accommo-

visual cells, transmutation dation, refraction

72, 169-70, 206 vision 270-1, 274 scleral ossicles

78 rhodopsin 289,293-5,321 visual fields

101-2 zapfensubstanz 299-300 binocularity

134-5, 138 origin, relationships 306-7 eye movements

145, 215, 342 habits 339-40 parietal eye

157, 161-2, 220-1, 224-5, 256-7 pupil 344-5 movement perception

174 acuity adaptations 423-4 adnexa

185-8 fovea 438 amphibious adaptations

191-6, 199-203 yellow filters and their 450-1, 454-9 spectacle

significance 465-7,495-7,519-20 color vision

223 Fig. 88 524-6, 538-43 dermal color changes

230 eyeshine 545-9 coloration of eye

The twenty families of lizards and the eleven families of snakes are
scattered around the globe in the temperate and torrid zones. Nothing
in biology is more certain than that the snakes were derived from lizards,
and the closeness of the relationship is indicated by the placement of
the two groups in a single order, the Squamata (meaning 'with scales')
as suborders, the Lacertilia (lizards) and the Ophidia (snakes).

Lizards — The lizards exhibit a greater number of the ocular features
listed earlier as 'reptilian' than do any other living reptiles. This does
not mean however that this combination of features was evolved first by
this relatively recent group — the absence of certain of them in turtles,
crocodilians, and Sphenodon has been explained above as owing to sec-
ondary nocturnality, to a special importance of the iris in accommo-
dation, etc. We may be sure that the lizards have only preserved, not
assembled, the complex here characterized (pp. 607-8) as 'reptiUan';
for, we shall encounter the entire complex again in the birds, which got
it not from the lizards, but from much older reptiles — the ornithischian
dinosaurs which were the birds' immediate ancestors.

The lacertilian eye is relatively large and characteristically 'diurnal'
in make-up, and has certainly been so for as long as there have been
lizards — and longer: If we could take the eye of Sphenodon in hand
and undo all of the things which have been done to make it suitable for
dim-light activity, we should find ourselves holding an essentially lacer-
tilian eye, representing not only the eye of the ancient diurnal rhyncho-
cephalians but probably that of the eosuchians as well (see Fig. 60, p.

THE LACERTILIAN EYE 623

135), To make complete the identity between the 'diurnalized' eye of
Sphenodon and that of the lizard, we should need only to pluck the
droplet-free cones from the Sphenodon retina.

The adnexa have been described adequately elsewhere (p. 423). The
eyeball is as high as it is wide except in the largest lizards, where it has
some horizontal ellipsoidality. The axial length is shortened somewhat,
and in diurnal species the circumcomeal region of the sclera is more or
less concave — supported so by the ca. 14 scleral ossicles, as part of the
means by which the ciliary body and the lens are brought into contact
for the purposes of accommodation. The thin scleral cartilage usually
reaches forward at least to the equator, often beyond, where it is met (or
a bit overlapped) by the broad, thin, ossicular ring (Fig. 182, p. 632).
In the chameleon, however, the cartilage is reduced to a four-millimeter
disc which lies behind the foveal region.

The circular cornea is usually of uniform thickness throughout its
arch (c/. Sphenodon) , and is relatively thin in large eyes, relatively
thick in small ones. Its sharp curvature continues for a little way into
the ossicular zone, before the sigmoid flexure of the ossicles reverses the
curvature to become the more gentle one of the posterior segment. The
usual layers are present except in some geckoes, where (e.g., in Hemi-
dactylus mabouia) there is no trace of Descemet's membrane or meso-
thelium.* At its margin, the corneal substantia propria separates briefly
into three laminae, the two outermost becoming the fibrous investment
and lining of the ossicular zone of the sclera, while the innermost blends
with the connective tissue of the iris-angle region and often serves as the
'tendon' of the ciliary muscle.

Except in the smallest eyes, the retina thins out very gradually toward
the ora terminalis (as in Sphenodon) , where the thin chorioid becomes
the ciliary body. This is very broad owing to the disparity between the
size of the posterior segment and that of the cornea. The base-plate
diverges slowly from the sclera, so that even at its anterior end the ciliary
body is not very thick (compare Sphenodon; contrast chelonians and
crocodilians) . The anteriormost strands of the meshwork tissue of the
iris angle may be organized as a pectinate ligament, but this is never as
well defined as in birds. There are no ciliary processes. Nevertheless,
the ciliary body has a broad zone of firm contact with the lens, which is

*Present, however, in Coleonyx — as one of the many reasons (ophthalmological ones, at
least) for considering this and other 'eublepharid' geckoes to be a distinct group with per-
haps only very distant kinship with the spertacled majority of geckoes.

624 REPTILES

thus directly squeezed equatorially when the ciliary muscle contracts
and moves the anterior end of the ciliary body forward and axiad (see
Fig. 109, p. 275, and Fig. 182, p. 632).

The ciliary muscles show great variations from lizard to lizard. Typ-
ically, perhaps, they are as described on pp. 277-80; but they are often
much simpler. In the Teiidse, for example, the muscle is all in one piece,
its purely meridional fibers originating from the corneal margin iv.s.)
and terminating in the base-plate and on the glass membrane. In noc-
turnal forms, the muscle may be massive or it may be greatly atrophied
as if the animal had abandoned all attempts to accommodate. The
muscle is tiny in Xantusia riversiana and in Hem'tdactylus mabouia, and
absent in X. henshawi, X. vigilis, and Heloderma siispectum. It is huge
in Coleonyx variegatus, however, and is well developed in Aniella pul-
chra considering the size of the eye. There are often special arrangements
which seem purposed to produce a nasad shift of the lens during accom-
modation, thus aiding the transversalis muscle (usually present) in
converging the visual axes. Thus in Seps and Lacerta, bundles of circum-
ferential fibers have been described and figured in the temporal half of
the eye (cf. Sphenodon) ; and in Tupinambis, though all the fibers are
meridional, they are much longer on the temporal side.

The iris is relatively thick, and often thicker toward the pupil, where
there is a vascular plexus fed by a temporal and an inferior artery and
drained by many radial veins. The sphincter is scattered through the
whole iris, and some of its fibers are bowed into radial positions and
must act separately, since no other dilatator is present. Where the pupil
is a vertical slit, the arrangement may be very complicated (see Fig. 88e,
p. 223). Both retinal layers are deeply pigmented. The zonule is very
thick where it attaches to the lens, and its anteriormost laminae run
parallel to the iris and so close to it that they suggest the origin of
the 'bridge-membrane' of Sphenodon.

The lens has an extremely thin capsule and is very soft, though not
so much so as in turtles. Its 'ringwulst' or annular pad is relatively thick
— in the chameleons, the thickest known. In the diurnal majority the lens
is flatter than in any other reptiles. The primary vitreous forms a broad
funnel, indicating that the slender hyaloid canal seen in turtles — though
these are the most primitive of living reptiles — is something special.

Pointing through the watery vitreous toward the heart of the lens is
the conus papillaris, a slender papilla rooted on the ventro-temporal optic
nerve head (Fig. 182, p. 632). It consists largely of tiny blood vessels

THE LACERTILIAN RETINA 625

with their surfaces heavily dusted with pigment granules, and among
these just enough neuroglial tissue to hold the whole together and in
shape. In cross-section the conus may be circular, oval, X- or Y-shaped —
in the latter cases, foreshadowing the buttressed 'pecten' of the lower
birds. It is supplied by an artery and a vein which reach it through the
optic nerve, and is one of the various devices which many vertebrate eyes
have found necessary for supplementing the disadvantageously-located
chorioid in the nutrition of the inner layers of the retina (see pp. 648-58) .
In profile the conus may be stubby, long and nearly cylindrical, or
dagger-like. In length, it varies from a nubbin in most nocturnal forms
(Xantusia, many geckoes) and sluggish species (skinks) to a third or
more of the diameter of the eyeball — in such instances, nearly reaching
the lens. It is completely lacking only in the various families of worm-
like, burrowing lizards (Amphisbaenidae, Euchirotidae, Anelytropidae,
Dibamidae*), whose tiny (less than 1.0mm.) eyes are buried beneath
(usually) opaque skin and seldom consist of more than a connective-
tissue capsule containing an optic cup and a lens.

The Lacertilian Retina — The outstanding feature of the retina is its
fovea centralis, which is not known to be lacking in any diurnal lizard.
The fovea may, as in chameleons, be larger than that of man, and with
a vastly greater concentration of visual cells (as many as 756,000/sq.
mm.). The fovea is absent, despite statements to the contrary, in all
geckoes which have ever been examined; and it is also wholly lacking in
pygopodids, Heloderma, and most xantusiids. In Xantusia vigilis, how-
ever, just enough trace of an area centralis has survived the family's
adoption of nocturnality to enable one to tell where in the retina the
fovea used to lie. The disturbance created in the average lizard eye by
the fovea scarcely finds scope to subside before the ora terminalis is
reached (see chameleon in Fig. 71, p. 173), and it is only in monitors,
iguanas, and the like that the retina has sufficient area to boast a wholly
unaffected 'extra-macular' peripheral zone of any great width.

In its laminal purity and in the thickness of its inner-nuclear and
ganglion layers, the lacertilian retina is exceeded only (and not greatly)
by the visually supreme birds. The pigment-epithelial processes are

*But not Aniella. The eyes of this Httle Cahfornian worm-lizard are a Httle less than a
millimeter in diameter, but they have all their 'works' — pigmented conus, normal retina and
visual cells, scleral ossicles, ciliary muscle, ringwulst etc. This genus is erroneously listed
in Table XI (p. 450) as having a spectacle. The lids are mobile, despite statements to the
contrary in herpetologica! literature.

626

REPTILES

numerous, long, and fine, but the pigment migrates so slightly that it
forms practically permanent sheaths around the individual cone outer
segments, as in diurnal snakes.

The visual cells are always of two types (each varying, of course, in
size), which form a 'matching' single-double combination (Fig. 180).

Fig. 180 — Visual-cell types in representative lizards, x 1000.

a, single and double cones of a diurnal lizard, Crotaphytus collaris.

b, single and double 'intermediate' elements of Xantusia river siana.

c, single and double, completely transmuted rods of a gecko, Coleonyx variegatus.

In the diurnal majority of families both of them are typical cones (Fig,
180a) with yellow oil-droplets, respectively homologous with the drop-
let-bearing single and double elements of all lower reptiles and the birds
and lower mammals — indeed, tracing their ancestry back to the chon-
drostean fishes (see Plate I). In the nocturnal 'leaf-footed'- or snake-
lizards (Pygopodidaj) of Australia, however, the oil-droplets have been
discarded and the outer segments somewhat enlarged to permit scotopic

THE OPHIDIAN EYE 627

vision. In Aniella and Heloderma the droplets are present though color-
less— which is true also of Xantusia, whose outer segments are rod-like
in size and shape (Fig. 180b). The geckoes have finished the job of
changing the ancestral cones into rods, whose outer segments contain an
abundance of rhodopsin and are either very long and slim as in
Coleonyx (Fig. 180c), or short and thick as in the spectacled geckoes.
A few genera of geckoes have secondarily (or tertiarily!) reverted to
round pupils and partial or perfect diurnality. These include Phelsuma,
Lygoddctylus, Pristurus, Gonatodes, Microscalabotes, Sphcerodactylus
(some spp.), and perhaps Teratolepis. All of these are candidates for
histological examination, which in some of them at least will unques-
tionably reveal that the visual cells have become 'cones' once more.

Snakes — Leaving out of account the 'blind' families (Typhlopidae and
Leptotyphlopidse) , in which the eye is tiny and vestigial, the eyes of
snakes are quite thoroughly standardized in structure. From genus to
genus (usually without regard to family boundaries) only minor vari-
ations occur, the most important of these being in the structure of the
retina, in the shape of the pupil, and in the relative size of the lens —
variations which, in short, are the bases of simple differences in visual
habits with respect to light intensity.

The presence of the spectacle cannot be held accountable for the
peculiarities of the eyeball other than the thin-ness of the corneal epithe-
lium. And these peculiarities are numerous and great: as the ensuing
description of the eyeball unfolds, the student who has just read the
preceding portions of this chapter will not recognize the snake eye as a
'reptilian' one at all; but, under a subsequent heading, an explanation
of the unique ophidian pattern will be offered which, it is believed, will
be entirely satisfactory.

The eyeball in life is spherical or even a trifle elongated axially. The
sclera is composed entirely of tendinous connective tissue. It is thickest
posteriorly, where, in average-sized eyes, it about equals the retina. In
the largest snakes (large boas, pythons) it is still thicker — up to one and
one-half times the thickness of the retina (e.g., Epicrates) . In very small
eyes, however, the sclera is usually very thin. The equatorial zone, where
the eyeball wall deforms most during accommodation, is almost always
(exception: Acanthophis) the thinnest portion of the sclera. It begins
to thicken again, as one passes forward, about at the ora terminalis, in
front of which it is quite thick for a little space, then thinned again at
its junction with the cornea. The outer surface of the sclera is usually

REPTILES

dotted with melanophores, and in a few instances these form a contin-
uous thin layer of dense pigment (Lichanura, Sonora, Abastor, Farancia,
Ndtrix, Acanthophis) . In Python (molurus) there are also many flat
pigment cells at various levels in the scleral tissue itself.

Fig. 181 — The ophidian eye in vertical section: Natrix natrix. x22.
Redrawn from Schwarz-Karsten, modified from original preparations.

am- accommodatory muscle; ap- anterior pad of lens; b- brain; c- cornea; cb- ciliary body
(main portion, the ciliary roll; note cross-section of hyaloid vein lying on orbiculus behind
it; the very small vessels of the hyaloid plexus, lying on the inner surface of the retina, are
omitted from the drawing); cr- cranium; cs- canal of Schlemm; hg- Harderian gland; io-
infraocular scale; s- sclera; sm- sphinaer muscle; so- supraocular scale; sp- spectacle; ^-
zonule (collapsed; see text).

The cornea is strongly arched and of almost uniform thickness except
— usually — toward its margin, where it is markedly thickened (the
'corneal thickening' hereinafter mentioned). This thickening is lacking
in many small eyes with thin scleras (e.g., Charina, Phyllorhynchus,
Hypsiglena, Trimorpbodon) , and even in the presence of a relatively
thick sclera, as in Tropidopbis (where the peripheral zone of the cornea
is actually thinned) and Eryx.

THE OPHIDIAN EYE 629

The chorioid is extremely thin (except in the limicolous 'rainbow
snakes', Farancia and Abastor), consisting of httle more than a chorio-
capillaris (with no large-vessel layer) and a few tightly-packed layers of
pigment cells external to it. In contrast to other reptiles, the chorioid
and sclera are firmly fused, as if they had never completed their embry-
ological differentiation from each other.

Anterior to the ora, the chorioid continues unchanged (including its
choriocapillaris) for a short space, where it is lined with the flat zone
of the tall ciliary epithelium. This 'orbicular' zone is always very narrow
(except in Python and Epicrates) , and upon it lies an annular 'hyaloid'
vein (except in boas; present, however, in Python). The orbicular zone
itself is lacking in Charina and Constrictor (= Boa) , and much reduced
in Lichanura. Immediately in front of the ora in these snakes, and an-
terior to the orbiculus in all others, lies the ciliary body proper, which
from its shape (Fig. 181) is perhaps best called the 'ciliary roll'. It forms
an annular fold, consisting of the two tall columnar layers of ciliary
epithelium with a core of deeply pigmented uveal tissue containing small
blood vessels. From this core, strands of connective tissue sweep for-
ward onto the inner surface of the cornea, petering out on the posterior
slope of the corneal thickening. These strands have much the same rela-
tionships as those which compose the corneal meshwork tissue of man
(see Fig. 5, mt; p. 10), which is so often mistakenly called a 'pectinate
ligament' : in both snake and man, the direction of these fibers is exactly
at right angles to that of a true pectinate ligament (see Fig. 109, pi;
p. 275).

The ciliary roll serves for the attachment of the zonule (v./.), and is
often taller and thinner (and sometimes sharp-edged) on the nasal side.
In Python and the larger boas {Constrictor, Epicrates) it has this shelf-
like character throughout its circular course.

In the Colubridze and all of the higher families derived from them,
the standard location of the venous canal of Schlemm is in the cornea,
toward the rear of the corneal thickening. It may be separated from the
anterior chamber only by the 'pectinate ligament' (c/. man!), but most
often it lies completely surrounded by dense fibrous tissue. It sometimes
branches (the branches then recombining) along its course and the sec-
ondary canals thus formed lie farther posteriorly, often in the core of
the ciliary roll. Its connections are chiefly if not solely with the chorio-
capillaris of the orbiculus. The Boidae show more variation : in Con-
strictor and Eryx no canal can be made out at all, and Lichanura, Trop-

630 REPTILES

idophis, Charina, and Epicrates have it as in the colubrids; but in Python
it is located closer to the outer surface of the cornea than to the inner,
and its connections are to the conjunctival veins.

The iris is fairly thick, with a highly irregular anterior surface. Its
stroma contains not only melanophores as usual, but often guanophores
and lipophores as well. The circulation is totally different from that in
lizards (p. 624) , consisting of a plexus occupying the whole iris, in which
the small vessels cannot be identified as veins or arteries. The striated
iris musculature is entirely mesodermal, and derived phylogenetically
and embryologically from the ciliary region. Most of the fibers are
circular in direction, and most of these are gathered into two accumu-
lations, one near the pupil and serving as the sphincter pupillae, and the
other toward the root of the iris and acting as the muscle of accommo-
dation. Some of the fibers of this latter muscle may be pressed back into
the ciliary roll. The dilatator fibers underlie the sphinctral masses, and
may also occasionally reach back into the ciliary roll (e.g., in Acanth-
ophis) . In diurnal snakes the pupil has a peculiar, special duty owing to
the absence of movable lids : during sleep it constricts, to facilitate visual
unconsciousness.

The lens, unlike that of lizards, has sutures; and it lacks the ringwulst
of other sauropsidans. Consequently it is not much flattened, and is
helped toward its subsphericity (flatness index 1.1 — 1.25) by an 'anterior
pad' except in Eryx and Charina (and perhaps all other boids, or at least
the fossorial ones) . Like a ringwulst, the anterior pad is simply a region
of the lens epithelium in which the cells are extremely tall instead of
cuboidal. Except in water snakes, whose lenses deform somewhat during
accommodation as well as moving forward, the lenses of snakes are
firmer than those of lizards or turtles.

The zonule is peculiar, and perhaps variable, in organization. In its
fullest development it consists of two radially-fibrous membranes. One
of these arises from the front of the ciliary roll and passes along the
back of the iris and over the face of the lens. The other is essentially
equivalent to an anterior hyaloid membrane of the vitreous, and arises
from the back of the ciliary roll and surrounds the back of the lens.
This posterior 'leaf is readily seen in some snakes (e. g., Bitis, Coronella,
Arizona), but in many it can be made out with difficulty or not at all.
The anterior 'leaf would appear to function chiefly in hauling the lens
promptly backward to its resting position upon the relaxation of accom-

THE OPHIDIAN EYE 631

modation (see pp. 282-3).* Since the back of the lens rests solidly
against the cupped vitreous, it would not seem to matter whether the
anterior limiting membrane of the latter flares out to attach to the ciliary
roll (forming a 'posterior leaf for the 'zonule') or coincides — as appar-
ently it often (or usually) does, with the anterior leaf. Where two leaves
are discriminable, there are practically never any other zonule fibers to
be seen between them, with attachments to the equatorial region of the
lens. A conspicuous exception however is Epicrates.

All snakes have a plexus of tiny blood vessels on the inner surface of
the retina,"^ fed by an artery which enters through the optic nerve, and
drained by the nasal and temporal arcs of the hyaloid vein (lying on the
orbiculus) into a mid-ventral trunk which passes back over the surface
of the retina to leave the globe through the optic nerve. This vein and
artery are clearly homologous with those which, in lizards, supply the
conus papillaris. And, in scattered members of every good-eyed family
of snakes, they supply a conus as well as a network of vitreal vessels.
But the 'conus' of these snakes has no genetic connection with the conus
or pecten of other sauropsidans, for its framework consists of meso-
dermal connective tissue — not of neuroglia. It is never large or dagger-
like, but most often forms a low mound, pigmented or clear, with a
brush of cuticular fibers which emanate from it in all directions to
disappear in the vitreous. It is longest and slenderest in Vipera berus
(where it is heavily pigmented) and Lampropeltis triangulum (where it
is colorless) ; but it is never relatively longer than the conus of a noc-
turnal lizard. The history of the ophidian 'conus' is best illuminated by
the fact that it is frequently much larger in embryos than in their adults,
and is often present in embryos whose adults lack all traces of it. More-
over, the development of the vitreal vessels goes hand in hand with the
ontogenetic retrogression of the conus : as the latter dwindles, the meso-
derm of its flared base creeps out on the surface of the retina, centrif-
ugally from the optic nerve head, and it is in this film of mesoderm that
the hyaloid plexus takes form. The embryological history of the conus-
artery is thus strikingly like that of the mammalian hyaloid (see p. 113
and Fig. 42a, p. 112).

*In life, the two leaves of the zonule diverge much more, toward the lens, than they are
shown doing in Figure 181 (p. 628).

tin Tdrbophis, these vessels are really embedded in the retinal tissue — some of them, quite
deeply, as in mammals.

REPTILES

The ophidian optic nerve is unique — for the Sauropsida — in its total
resemblance to that of Neoceratodus (p. 591). The lacertiUan nerve is
also fascicular, but its bundles lack ependymal cores and have more glial
tissue between them.

sphincter, dilatotor

^^ Iris

^^....----^^^^orner;;^--^^

\ /v-

.y^ ^~^

\^Ni(^ Conalof Schlemm

My-

y'\ ^-r-mrciXEirraxn-r.,^ /"

X\ / ''" sclera)

}C \v(. Ciliary processes
^^,^\^^^v / locking

^^..^--— — -^

Base plate y^^^n^'^/^^

f

"^^^On^^^. Scleral ossicle

/^^?^

1

Wj^^---"-

Lens
(colorless)

^^^^^y^^^^%

^ ^^^^

iql ^^ bo°d'y

Ectodermal

^ Ringwulst XtA

\^

^ Vitreous b.

Fovea

/#

/ Optic nerve

^^^VOsclero (cartilagd

i^^^ yChorioid

^Retina (ovosculor
a with standard

"^^^21^^^^^^^^

f "/^

^\^ /

double cones)

^^

Yellow cone oil droplets

Fig. 182 — Lizard eye, diagrammatic, for comparison with that of snake.
(The dotted arrow shows the direction of application of the force of accommodation).

The History of the Snake Eye — If the reader needs any reminder of
the magnitude of the difference between the snake eye and that of the
ancestral lizard, it will be furnished by Figures 182 and 183. Herpetol-
ogists and palaeontologists are agreed that the snakes originated from
the stem of the lizard family Varanidae, the 'monitors'. These are the
largest of all lizards, and include the twelve-foot dragon of Komodo.

HISTORY OF THE OPHIDIAN EYE

633

The largest snakes — including the monster of them all, the 35-foot regal
python — are in the most 'primitive' family, the Boidae.

If big monitors had simply 'become' big snakes, there would have been
no need whatever for such a rebuilding of the eye as has occurred in the

Introconjunctival spaca

-Sclera (fibrous)

^Choriold

!tino(wlth

lique double

cones)

No cone oil droplets

No epichorioidal lymph spaces

Fig. 183 — Snake eye, diagrammatic, for comparison with that of lizard.
(The dotted arrow shows the direction of application of the force of accommodation).

Ophidia. The modern snakes would have done just as well with unmod-
ified lacertilian eyes as have the various imitation snakes — the legless
above-ground lizards such as our Ophisaurus ventralis and the European
Anguis fragilis. Earlier in this volume it was noted that the universal
presence of the spectacle, in snakes of all habits and habitats, could only
mean that the first snakes so lived as to require a spectacle : they were

634 REPTILES

either nocturnal, or else lived underground, and those of their descend-
ants which are neither nocturnal nor fossorial have been unable to trade
the spectacle in for a pair of mobile lids. Again, the absence of retinal
oil-droplets in all snakes, and the presence instead of a yellow lens in
diurnal species, has been emphasized as indicating that the early snakes
shunned bright light. Their invention of the spectacle and their discard
of the oil-droplets had a common basis.

Mere above-ground noctumality would not, however, have called for
any greater changes in the ancestral lizard eye than have occurred in the
night-lizards, snake-lizards, and geckoes. The pattern of the whole snake
eye is consistent only with the hypothesis that the first snakes lived
underground or originated there from lizards which had become fos-
sorial. Two whole families of snakes and several families of lizards have
this habit even today.

Quite aside from the structure of their paired eyes, there are a number
of other ophidian peculiarities which seem puzzling when one considers
how much alike the habits of snakes and lizards are, but are at once
explained by the fossorial-origin hypothesis: it accounts nicely for the
loss of not only the limbs but the ears as well, and the parietal eye,
dermal color-changes, retinal photomechanical changes,* and some of
the same cranial elements which are lacking in the subterranean amphis-
baenid lizards. All of these things are present in the Varanidae, and all
would certainly have been retained by the snakes if they had originated
on the earth's surface.

As the lizard ancestor took more and more strongly to an under-
ground life, its eye probably at first increased in sensitivity. The pupil
may even have become a slit, as it is in burrowing boas; and the retina
would in any case have lost the oil-droplet pigment, then the droplets
themselves, even if the cones were not converted temporarily into rods.
The long persistence of the light-shunning habit would permit the de-
generation of the whole apparatus of accommodation — and this com-
prises a good part of the eye : the atrophy of the ciliary muscle made it
no longer necessary to maintain a ringwulst, or scleral ossicles, or even
scleral cartilage; and of course the ciliary processes were already gone
in the diurnal lizard ancestor. As the eye shrank, then, it also became
spherical. The spectacle had to be provided early — though as the eye
degenerated beneath it, it eventually lost its usefulness for a time. The

*Though this meant only a hastening of a degradation which is seen in all other reptiles
as well (see Table II, p. 150).

HISTORY OF THE OPHIDIAN EYE 635

Harderian gland ballooned, as it has in caecilians and blind lizards;
and — as also in these forms — the lacrimal gland disappeared.

The loss of the fovea and the simplification of the retina involved
the optic nerve, which became slender and lost its septa; and the ecto-
dermal conus papillaris vanished along with the need for it. The pupil
lost all mobility as the iris muscles disappeared, and the chorioid and
sclera coalesced as in rudimentary eyes in general. The canal of Schlemm
shrivelled; and the eye finally 'touched bottom' in a condition not much
if any better than that of a modem Typhlops. Indeed, the organization
of the Typhlops eye is such that this worm-like form could well have
been the 'first' snake (see Plate I).

How long the snakes lived underground, no one can say; but they
did not (or did not all) remain there. Coming back to the surface, they
were under the necessity of reconstituting their eyes almost 'from scratch'.
The vestigial nubbins of visual cells had to be nurtured into bloom as
respectable rods. Then, as the race became better able to stand the light,
the retina became duplex. The eye enlarged, but in the absence of stiff-
ening structures in the sclera it was forced to remain forever spherical.
With the ciliary body and the lens now far out of contact, an entirely
novel means of accommodation had to be devised. The remnants of
ciliary muscle moved into the iris to play a dual role in accommodation
and in the operation of the (slit?) pupil.

The recrudescent retina demanded a better nutrition than the thinned
chorioid alone could supply. So, the snakes developed a mesodermal
conus papillaris, but shortly abandoned this in favor of the more 'direct'
vitreal vessels (a change from which the lizards — and the birds — would
probably profit if they could make it; see pp. 653-4). They also pro-
duced a new 'canal of Schlemm', in a new location and with new con-
nections to the venous system, and elaborated a whole new circulation
for the iris (which, if we can go by the caecilians, probably had no meso-
derm left in it during the underground period). And when (in the Col-
ubridae) the retina finally became pure-cone, with new and unique double
elements, supporting a diurnality as thoroughgoing as that of any lizard,
the needed yellow filter was manufactured out of the lens itself. With
a high ratio of optic nerve fibers to visual cells once more restored, the
optic nerve became too plump to remain a simple cord, and an entirely
new system of fasciculation and septation was invented for it.

The resulting eye — as we see it today — presents substitutes for all
the losses, remedies for all the defects, of the vestigial organ of the

REPTILES

original snakes. And these losses and defects were so numerous that the
snakes had almost to invent the vertebrate eye all over again. Nothing
like this tremendous feat has occurred in any other vertebrate group,
so far as we can tell. No other vertebrates except the placental mam-
mals* have had to do any 'rebuilding' at all. Wherever else the eyes have
degenerated, they have remained degenerate as long as their owners
survived. We can perhaps understand now why a legless lizard is not a
snake simply because it is legless. The snake-shaped lizards such as
Ophisaurus and Pygopus originated above-ground, and escaped the pain-
ful period of near-extinction which the true snakes experienced and
which they have so gloriously survived.

The Ophidian Retina — Apart from the visual-cell layer, the strata
of the modern snake retina are quite orthodox
in structure, and it is unlikely that they have
undergone any drastic reconstruction as a con-
sequence of the underground babyhood of the
Ophidia; for, wherever the eye has become
vestigial but has retained a functional retina
(e.g., in cascilians), one notes that though the
visual cells are reduced to nuclei each bearing
a mere knob of cytoplasm, the nuclear and
plexiform layers are still present and distinct.
The phylogenetic steps between the Typh-
lopi-[\ke condition and the mammalian-like
retina of the Boidas are lost, and we can only
guess at them (Plate I) . The boas and pythons
all have the same retina, exemplified in Figure
184 by Tropidophis, which has only single
cones and rhodopsin-bearing rods. The cones
here (as in all snakes) lack not only oil-drop-
lets but also paraboloids and myoid extensi-
bility. In all these respects, they indicate
plainly that they were never derived directly
from above-ground lizard cones.

Between the Boidse and the great central
family Colubridse there is again a great gulf,
which may be partly filled if ever the retina of

And perhaps the cod family (see pp. 398-9, and footnotes on pp. 586 and 588).

O.N

fe €'

(?)

•G.

Fig. 184 — Retina of one of

the Boidse, Tropidophis mel-

anurus. x 500.

P.E.- pigment epithelium; R.-
rods; C.- cones; L.- Limitans;
O.N.- outer nuclear layer;
I.N.- inner nuclear layer; G.-
ganglion-cell layer.

THE OPHIDIAN RETINA 637

the osculant Xenopeltis comes to histological examination. The 'stand-
ard' colubrid retina is pure-cone, with three types of elements, only one
of which (Type C) has the structure and staining behavior of the boid
cone; and this type is present only in small numbers at best (Fig. 185a).
It was probably the progenitor of the abundant Type A single cone
(see Plate I), which in turn somehow gave rise to the unique ophidian
double cone (Type B; see Fig, 24, p. 59).

Fig. 185^ — Representative visual cells of diurnal and secretive colubrids. xlOOO.

(Here, and in the illustrations on the next two pages, the hoinologous elements are labelled
with capital letters designating their type; see text).

a, the three cone types present in all diurnal colubrids and elapids (except where Type C
has been discarded; see text); drawn from Natrix natrix.

b, visual cells of the scarlet snake, Cemophora coccinea, exemplifying a number of secretive,
crepuscular, and semi-nocturnal colubrids. Note enlargement of the outer segments, and
tendency of Type C toward a rod-like form (c/. C in Fig. 187).

It is interesting — in fact, fascinating — to note that with their pro-
duction of this diurnal colubrid arrangement, the snakes had at last
struggled back to a pattern which strikingly simulates that of the archaic
reptiles : single and double elements which match in structure, plus an
'odd man' in the form of the Type C cone. And, the snakes have
wandered off into nocturnality by various pathways, for the Type C
cone, like the droplet-free cone of the cotylosaurs and eosuchians, has
shown itself to make a better rod than a cone:

In those diurnal colubrids and elapids which exhibit high visual acuity,
the Type C cone has been eliminated and types A and B are slenderized

638

REPTILES

^ip:i#3|i

and aggregated {Malpolon, Dryophis, Sepedon*). In secretive, crepus-
cular, and some nocturnal colubrids (e.g., Lampropeltis, Rhinocheilus,
Arizona, Cemophora, Trimorphodon) the outer segments of types A

and B are more or less enlarged and
tend toward a cylindrical form; but
the Type C element is even more rod-
like— leads the way, so to say (Fig.
183b). In another assemblage of noc-
turnal colubrids (Tarbophis, Dasy-
peltis, Leptodeira, Dipsadomorphus,
etc.) the Type C element has become
a perfect rod and contains rhodopsin,
but the other two elements have outer
segments which are no more than
intermediate between diurnal-colubrid
cones and full-fledged rods (Fig.
186). Moreover, the A and B types
in these forms are much elongated,
as if to put them in the background
not only topographically but physiol-
ogically. In nocturnal elapids (coral
snakes, kraits, etc.), simulations of
these various nocturnal colubrid pat-
terns occur, with the Type C element
again leading the trend toward sec-
ondary rod-hood.

A very few nocturnal colubrids (e.
g., Hypsiglena, Phyllorhynchus [and
Lytorhynchus?]) have converted all
three cone types into massive cylin-
drical elements (Fig. ISV^) — perhaps
the most spectacular of transmuta-
tions, but actually a simple one since
these secondary rods lack rhodopsin,

*These forms, when compared with the other members of their families, thus afford an
interesting comparison with the lizards: these snakes, and the lizards, have both striven for
maximal visual acuity by eliminating the poorest of three cone types — one which makes a
good rod, but a somehow poor cone.

tThe single and double rods here have no definite mosaic arrangement in the retina, whereas
in geckoes the single and double rods form alternate rows running horizontally of the eyeball.

Fig. 186 — Retina of Leptodeira annu-

Idta, exemplifying the Tarbophis series

of nocturnal colubrids. x 500.

A- single cone (Type A element); B-
double cone (Type B element); C, C-
layer of rods (Type C elements); o-
outer nuclear layer; /- inner nuclear layer;
g- ganglion-cell layer.

THE OPHIDIAN RETINA

639

and the retina owes as much of its sensitivity to increased summation
as to the lowering of the thresholds of the individual visual cells.

Fig. 187 — Representative visual cells
(transmuted rods) of a nocturnal colubrid,
Hypsiglena o. ochrorhynchus. xlOOO.

Fig. 188 — Visual-cell types in the Cro-

talidcP: single cone, double cone, and

rod; from the copperhead, Agkistrodon

mokasen. x 1000.

a b

Fig. 189 — Representative visual cells in the Viperid« (see text). xlOOO.
a, of Cape viper, Causus rhombeatus. b, of puff adder, Bitis arietans.

640 REPTILES

In the vipers (Viperidae) and pit- vipers (Crotalidae), derived inde-
pendently from colubrid ancestors, the diurnal colubrid pure-cone pat-
tern has again been taken over and converted into a duplex one by the
transmutation of the Type C cone into a rod. All of the Crotalidae
(moccasins, rattlesnakes, fer-de-lances) show the pattern of Figure 188,
with the rods outnumbering the cones about as extensively as in man.
The viperid retina is rather more complex. The primitive vipers (Causus,
A tract as pis) are crepuscular and have nearly-round pupils. The Causus
retina (Fig. 189a) looks at jfirst glance like a diurnal colubrid one to
which a few rods (C) have been added. The retinas of the highly
specialized vipers (Cerastes, Bitis, et al) show the same four types of
cells (Fig. 189b) ; but here the C' rods outnumber the combined cone
types by three to one (in sections). The mystery of the C' elements
clears up when one looks at the retina of the central genus of the family,
Vipera. In V. berus the Type C cones and the Type C rods intergrade
structurally through an unbroken series of intermediate conditions.
Causus and Bitis have obtained their four types of visual cells simply by
getting rid of the intermediates between two of them, which Vipera —
fortunately for the comparative retinologist — ^has never eliminated.

Two colubrid genera, Farancia and Abas tor, resemble Vipera closely;
but this is of course no implication that the Viperidae stemmed from such
colubrids, any more than the essential similarity of the crotalid and
Leptodeira patterns implies a genetic relationship.

The plasticity of the ophidian retina is thus enormous. The snakes
alone have rung as many changes upon their visual-cell patterns as have
all the other vertebrates put together (Plate I). If anything could make
a snake-hater learn respect and admiration for this abused group of
animals, it would be the study of their eyes. The writer speaks from
personal experience!

Chapter 17
BIRDS

See also pages:

47 Fig. 21b

50, 178 amacrine cells

79, 127-8 photosensory ependyma

102 zapfensubstanz

102 Fig. 35

1 18-9 embryology

134-5, 139 origin, relationships

150, 156, 162 photomechanical changes

156, 158, 162, 220-1, 226 pupil

169-70, 172-4, 205-9, 307-10, 341-2,

344-5, 438-42 habits, visual acuity
176, 215-6 visual cells
179-80 blind spot

182 Fig. 75 b

183 Fig. 76

187-9, 307-10, 324, 442 area centralis,
fovea;

192-7, 200-1, 203 oil-droplets and their

significance
212-3 tubular eyes
230, 240-1 eyeshine, tapetum
251 Fig. 100
257, 269-82, 438-42 accommodation,

refraction
274 scleral ossicles
289-91, 295-6, 300, 307-10, 320, 323

visual fields
307-10, 329 eye movements
307-10, 320, 323-4, 327, 331 binocularity
339-40 median eyes
341-2 monocular stereopsis
344-5, 354, 365-7 movement perception
419-25 adnexa

438-42 amphibious adaptations
466,497-504,519-20 color vision
524 dermal color changes
545-51 coloration of eye

The avian eye contains no feature of any importance which does not
also occur in some reptiUan group, and practically all of its features
occur in the lizards — not because the birds came from lizards (their an-
cestors were certain of the dinosaurs), but because nothing material has
needed to be changed, in the eye, during the descent of the lizards and
birds from their immensely remote common ancestors, the eosuchians.

Though the birds comprise a whole vertebrate class, containing thou-
sands of species divided among many orders, the eye is as uniform
throughout the group as it is in any one order or suborder of reptiles
or amphibians.

The Eye as a Whole — The great size of the bird eyeball — the primary
basis of the paramount eye-mindedness of the group — ^goes unrealized
by the casual observer, for only the relatively small cornea shows in the
circular lid-opening. Only the tiniest of birds, such as hummingbirds,
warblers, and finches, have eyes as small (6-8mm.) as those of the aver-

641

642 BIRDS

age amphibian or reptile. The two eyes of a bird often outweigh its brain,
and there is often barely room enough for them in the head. The largest
land-vertebrate eye is that of the ostrich, 50mm. in diameter. Hawks and
owls, a fraction of the size of a man, have eyeballs as large as ours and
larger.

Such eyeballs are necessarily a tight fit for their orbits. There is no
room for a muscle cone like that of a shark or a man. The reptilian re-
tractor bulbi muscle has been discarded — leaving behind it, however,
its derivative, the bursalis (see Figs. 142b, 143c and f; pp. 420-1). The
oculorotatory muscles are ribbon-like, and plastered snugly against the
globe (Figs. 70, 107d; pp. 172, 270). They never extend forward beyond
the limits of the convex posterior portion of the eye; hence, where the
latter is tubular (Fig. 190c), the muscles are relatively short (and, in
owls and some eagles, functionless) .

The shapes of avian eyes fall into three rough categories : flat, globose,
and tubular (Fig. 190). In all, however, there is a prominent concave
region which coincides with the zone occupied by the ciliary body and
the ring of scleral ossicles which creates and supports the concavity. In
the 'flat' eyes exhibited by a very great majority of birds, the axis is much
the shortest of the three diameters, equalling but seven- or eight-tenths
of the vertical. The shape of these eyes is thus the same as in the lizards.
In those diurnal birds which need high resolution at great distances (i.e.,
wing-feeding insectivorous forms, predators in general, and such types
as the crow) , the ratio goes as high as unity, yielding the 'globose' form
of eyeball. In most owls (and some eagles) the axis is as long as the
other diameters or even a bit longer, and at the same time the concave
zone is so broad that the eye is rendered 'tubular'. In these instances the
retinal area is relatively small; but the retinal image may be either small
(where the lens is closer to the retina and rotund — owls) or large (where
the lens is farther forward and flatter — eagles). Accompanying the in-
crease in relative axial length one sees invariably a proportionate broad-
ening of the curvature of the posterior segment, so that the junction of
this region with the concave zone becomes more and more conspicuous.
Except where the lens recedes into the eye and sharpens its curvature
(as in owls, Podargus, etc.), the phylogenetic increase in the axial length
of the bird eye can always be described as adaptive toward the securing
of higher visual acuity, through an increased 'throw' of the image from
optical center to retina and the consequent broadening of the image at
the visual-cell level.

THE AVIAN EYE

643

Horizontal ellipsoidality is slight at most — the ratio of the horizontal
diameter to the vertical is usually 1:1 and never greater than 1.2:1,
But nasad asymmetry is universal: the cornea and lens are not only
tilted toward the beak, but shifted in that direction as well (Fig. 190;
Fig. 71, p. 173). This effort to secure a maximal overlapping of the
monocular visual fields is just as great, or greater, in elongated eyes
whose retinae and visual fields are restricted by their tubularity.

The sclera always contains a hyaline-cartilage cup, which extends for-
ward to the back edge of the ossicular ring, where it is usually locally

Fig. 190 — Bird eyes, showing charaaeristic shapes, xl. After Soemmering.

(Each drawing shows the ventral half of the left eyeball; the nasal side is to the right;
the plane of the ora terminalis retinae has been placed horizontally to bring out the nasad
asymmetry which is present to some degree in the eyes of all birds).

a, commonest, 'flat' type (in a swan, Cygnus olor). b, 'globose' type (in an eagle, Aquila
chrysaetos). c, 'tubular' type (in an owl, Bubo bubo).

thickened. External to the cartilage is a dense fibrous layer, often as thick
as (or thicker than) the cartilage itself, particularly in the fundus and
particularly in large eyes. Surrounding the optic nerve there is often
(most often in small eyes*) a plate of bone, the 'Gemminger's ossicle'.
This may be horseshoe- or washer-shaped, or may be represented by sev-
eral separate pieces. It is set in the cartilaginous cup as if formed from
a portion of the latter's substance; but its mode of development is un-
known, as is also its physiological value. The anterior scleral ossicles

*And supposed to be conspicuously developed in the woodpeckers; but it is lacking in the
flicker.

644 BIRDS

(Fig. 107, p. 270) overlap the scleral cartilage externally (Fig. 191),
and extend forward nearly to the limbus. Their number ranges from ten
to eighteen, except for rare instances among diving birds, where the
basic number has been increased by anterior and posterior fragmentation.
Fifteen is the commonest number and perhaps the 'original' one. In a
summary of 460 species of birds, Lemmrich found the ossicle numbers
to be distributed as follows :

No. of ossicles: 10 11 12 13 14 15 16 17 18
No. of species: 1 18 26 57 138 182 31 3 4

Though the ossicle of Gemminger, despite its thinness, usually or al-
ways contains marrow spaces, such are present in the anterior ossicles
only where these are largest and thickest (owls, frogmouths, hawks,
eagles, etc.). The fact that the bony ring is made up of separate pieces
probably has no physiological significance, but Lemmrich has pointed
out that the ring could not otherwise grow with the eyeball.

The cornea is usually relatively small in area, and especially so in
underwater swimmers; but it becomes larger in globose eyes and very
large and strongly arched in nocturnal forms. It is ordinarily somewhat
thinner at its apex than at the periphery, but in large eyes the thickness
of the cornea tends toward uniformity everywhere. In spite of its cus-
tomary eccentric position, it is almost always circular in outline and
neatly fills the lid opening. Histologically, the avian cornea is quite like
that of man, though a Bowman's membrane is not always differentiated.

The corneal surface is kept especially well polished by the action of
the nictitating membrane with its lining of papillose cells. The nictitans
also cleans off the inner surfaces of the other lids, and keeps them from
smearing the cornea, in those birds in which the lids close just after the
nictitans in a 'blink' (e.g., pigeon). The nictitans has a marginal pleat
which slides easily under the lids in the 'going' direction, but scrapes
them on its way back. In many birds or most, the lids close only in sleep
and the nictitans alone blinks. In consequence, the upper and lower lids
have a largely unstriated, slow-acting musculature.*

The chorioid is relatively thick — more so than in mammals and much
thicker than in reptiles. It is thickest in the fundus. Its distinct vessels
appear to be mostly arteries, and these lie close to the choriocapillaris
which they supply. Between them and the thin, pigmented 'lamina fusca'
(applied loosely to the sclera) lies a thick region which in prepared slides

*In altricial birds the lids are closed for a time after hatching, but in all birds they are wide
open before hatching, not fused edge-to-edge as in fetal mammals.

THE AVIAN EYE

645

appears largely empty, but actually has a sinusoidal (lymph? venous?)
structure. Traversing this thick open layer, with their direction radial
with respect to the eyeball, there are connective-tissue cords and columns
which often contain (or consist largely of) muscle cells. These may be

fC/Vs

S0'~-

^bm

-bp

ch.

'•sr

Fig. 191 — The ciliary region of a bird eye.

(Semi-diagram of the temporal quadrant in the red-tailed hawk, Buleo h. borealis. Blood
vessels, including the canal of Schlemm, omitted).

ap- annular pad or ringwulst of lens; bp- base-plate of ciliary body; c- cornea; ch- chorioid;
cm- Crampton's muscle; co- conjunctiva; cp- ciliary process; «- iris; lb- lens body; ot- ora
terminalis; pi- pectinate ligament; s, s- sclera; sc- scleral cartilage; so- scleral ossicle; so'-
overlapped portion of adjacent scleral ossicle; sr- sensory retina; icm- tendon of Crampton's
muscle; //- tenacular ligament; z- zonule.

smooth or striated, and their contraction would obviously thin the chor-
ioid temporarily and draw the retina backward. In the flicker (and other
woodpeckers?) the chorioid is not empty-looking, but contains a thick
mass of mucoid tissue which has probably been developed to prevent

646 BIRDS

a repeated forward movement, and detachment, of the retina during
'wood-pecking'. The chorioid in most birds is highly ductile in the direc-
tion of its thickness, i. e. radially of the globe : Abelsdorff and Wessely
found that if the anterior chamber of a bird is drained by corneal punc-
tures, the chorioid will promptly thicken enormously through engorge-
ment.

The avian chorioid is not known ever to contain a tapetum lucidum,
though some old accounts, not since substantiated, mention one for
certain owls. The eyeshine of the goatsuckers (nighthawks, whip-poor-
wills, etc.) is so vivid however that the eyes of these birds, for this and
other reasons, seem most attractive objects for study.

Anteriorly, the chorioid thins out and becomes the base-plate of the
ciliary body (Fig. 191), which angles sharply inward toward the axis
and leaves a large space between itself and the sclera, to be traversed by
the many strands of the pectinate ligament. The ciliary processes occupy
the whole ciliary zone (so that there is no true orbiculus) , and are very
numerous — sometimes numbering in the hundreds, though only a major-
ity are tall enough to reach the lens capsule and fuse therewith. The
number of processes goes roughly with the size of the eye, and from eye
to eye they do not vary greatly in thickness. From the ciliary processes,
and from between them, there originate the fibrils of the zonule, the
anteriormost of which are squeezed between the iris and the ringwulst,
as in lizards.

The ciliary muscles, as in lizards, are more closely associated with the
sclera than with the uvea. They may be arranged as in Figure 191
or, probably much more commonly, the muscle of Briicke originates
from the inner side of the thin scleral sheet which forms the anchorage
of the pectinate ligament and covers the inner side of Crampton's muscle.
Briicke's muscle is sometimes divided into an anterior and a posterior
portion; then, the anterior is properly known as 'Miiller's muscle' — first
described by Miiller in the goshawk, Accipiter gen tills . Other variations
are mentioned on pp. 279-81 and 439-42.

The 'canal of Schlemm' is complex, represented not by a single venous
annulus, but by two, with moreover an associated artery which lies be-
tween them (in Passer domesticus, two arteries), and has a likewise
annular course. The connections and relationship of the veins and
artery (s) are not yet known. The whole complex lies near the limbus,
attached by connective tissue to the inner surface of the sclera near the
anterior end of Crampton's muscle.

THE AVIAN EYE 647

The iris is often extremely thin just at its root, where the anteriormost
pectinate-Ugament fibers attach, like a zonule of the iris. Here the iris
may be reduced to little more than the retinal layers.* It promptly
thickens greatly, then slowly tapers toward the pupil margin where it
often has a knife edge (in contrast to the lizards; but c/. Sphenodon).
Sphincter and dilatator fibers, all striated, are distributed throughout
the width of the iris. These originate embryologically from the anterior
retinal layer at the pupil margin. Their action, like that of the avian
ciliary muscles, is extremely rapid. Both retinal layers of the iris are
pigmented; but a second dilatator system, identical in genesis with the
dilatator of mammals (and with its elements probably unstriated and
perhaps syncitial) , has been described by so many investigators that its
existence in at least some birds cannot be categorically denied. The
circulatory pattern of the iris is much as in lizards, with a wide plexus
of capillaries supplying the sphincter and drained peripherally by short
radial veins. Small vessels are concentrated near and at the anterior
surface of the iris, from which many of them protrude (as in many
reptiles and amphibians). Here also is concentrated the stromal pig-
mentation, which may incorporate many types of cells — particularly
lipophores. There is no unbroken layer of mesothelium on the face of
the iris. Though it literally squeezes the lens only in certain amphibious
birds, the avian iris is always of material assistance during accommo-
dation, in holding back the lens against which it presses, and in inhibit-
ing the peripheral part of the anterior surface of the lens from bulging,
thus concentrating the change-of-curvature in the part of the surface
opposite the pupil.

The lens is as highly refractive as in mammals, often more so, though
it is often very soft, particularly where the range of accommodation is
great. As in most of the higher vertebrates, the anterior surface is less
sharply curved than the posterior. It is flattest in most diurnal birds
(index 2.2-3.0), roundest in crepuscular and nocturnal forms, and in
divers (1.2-1.85). The annular pad or ringwulst is ordinarily well de-
veloped, and as a maximum (in Apus) it may take up half the area of
a sagittal section of the whole lens. In general, its relative thickness goes
with the capacity for accommodation, but it is very thin in diving birds
(loons, murres, cormorants, etc.), particularly in those whose iris sphinc-

*In captive owls which have been roughly handled, one sometimes sees an irregular second
pupil at the periphery of the iris, held open by the tonus of the sphincter. Such a defea is
not a 'coloboma', of embryonic origin, but has been produced by a local traumatic rupture
of the iris root, which is especially delicate in these birds.

648 BIRDS

ters do more of the labor of accommodation than their ciliary apparati.
The ringwulst is small also in flightless birds (Apteryx, ostriches) and
smallest of all — practically non-existent — in the Australian terrestrial
goose Cereopsis.

Between the ringwulst and the lens-body there is a slender space, a
vestige of the cavity of the embryonic lens vesicle (see Fig. 40e and f,
p. 1 10) , into which the inner ends of the ringwulst fibers secrete a fluid
substance. This perhaps serves only to lubricate the interface between
the ringwulst and the lens proper as the two shift past each other during
the accommodatory deformation of the lens. But it has been suggested
that there may be enough of the fluid to make a sharply-curved blister
under the anterior lens epithelium, when the fluid is squeezed forward
by the pressure of the ciliary processes. A 'bump' does form on the
anterior face of the accommodating lens, but this may be wholly due
to the mechanics of the lens and ringwulst and the orientations of their
respective fibers, and to the restraining pressure of the iris (v.^.) That
the sphincter contracts (stiffening the iris) during accommodation is
indicated by the tautening of the pectinate ligament, demonstrated
beautifully by Wychgram (and see Fig. 109, p. 275).

The Pec ten, and Its Analogues in Other Vertebrates— Tht most
conspicuous and perennially interesting feature of the avian eye is its
pecten (Fig. 192; see also Figs. 80 and 114, pp. 188, 308). The pecten
projects into the vitreous in the ventral half of the eye from the head of
the optic nerve, with which its base roughly coincides. It consists largely
of small blood vessels (of greater than capillary size). If these be con-
sidered comparable to the vascular supply of organs in general, then
the pecten must be described as an essentially ectodermal papilla, for
its scant framework is composed of neuroglial cells of optic-cup origin.
It is always pigmented (though occasionally only lightly), with the
pigmentation progressively deepening toward the apex of the structure
and heaviest of all in the 'bridge' which ordinarily binds and caps its
free end. The vascular supply of the pecten has no connection with that
of the chorioid, but its chief veins and arteries are probably homologous
with those which supply the falciform process, hyaloid or vitreal vessels,
conus papillaris, and retinal vessels of fishes, amphibians, reptiles, and
mammals.

Two types of well-developed pectens occur; their morphological and
genetic inter-relationships are obscure. The palseognathous birds, which
are primitive and (except the tinamous) flightless, characteristically have

THE PECTEN AND ITS ANALOGUES

649

a pecten exemplified by that of the ostrich, Struthio camelus (Fig.
192a). Here the organ has a central vertical panel which is buttressed
along its sides and ends by lateral vanes (Fig. 192c). The same plan
is followed by the 'American ostrich' (Rhea) and apparently by the
tinamous. The situation in the emu (Dromceus) is unknown; but in the

Fig. 192 — The peaen.

a, peaen and optic disc of ostrich, Struthio camelus. x5. After Franz.

b, portion of eyeball wall bearing pecten of domestic fowl, exemplifying type present in
most birds. x8. After von Szily.

c, section of a near, and parallel to, its base, showing central web and lateral vanes. After
Franz.

d, section parallel to base of pecten of red-tailed hawk, Buteo b. horccilis, showing pleated
structure characteristic of the common type of pecten shown at b. x7.

b- 'bridge' which cements folds distally; d- dorsal end of peaen.

650 BIRDS

cassowaries {Casuarius spp.) the pecten is built as in the neognathous
birds :

The Neognathae* all have the pecten organized as an undulant or
accordion-pleated fin, superficially resembling an ordinary steam-heating
radiator (Fig. 192b, d). The pleats of such a pecten, when it has been
excised, can be smoothed out and the whole organ rendered plane, but
only after the apical bridge has first been cut away. The basal area of
the organ, the extent to which its ventral end is free of the nerve head,
the number of its folds, and the closeness of its approach to the ventral
ciliary body and to the ventral periphery of the lens, are all subject to
great variation. Its location is constant, however — in all birds the long
axis of the base of the structure is directed along the former course of
the embryonic fissure of the optic cup; for, since its glial framework
develops from the head of the optic nerve, it necessarily conforms to
the fissure as does the elongated head of the nerve itself.

One of the flightless genera of palaeognaths, that of the kiwis {Ap-
teryx) , has a pecten which is really a conus papillaris, identical with that
of many a lizard (see Fig. 182, p. 632). The eyeball of this large noc-
turnal bird is only 8.0mm. in diameter and in axial length. The slim
pecten is reported to be 2.0mm. tall and 0.3mm in diameter along its
shaft; there are no vanes or pleats. It would be natural to suppose that
the kiwi pecten is primitive, and links the vaned and pleated pectens with
the simple ancestral reptilian conus papillaris. Such an interpretation is
denied us: the kiwi eye — including its pecten — is as degenerate as it is
possible for an avian eye to be. It is myopic and affords its owner only
very poor vision both by night and by day; and it is tiny, whereas the
orbit is huge — implying that the eye has dwindled greatly in size.
According to Kajikawa, the eye accomplishes no growth whatever be-
tween the 'hen-sized' juvenile condition and the 'turkey-sized' adult
stage.t The kiwi, unlike all other birds, appears to have a good sense of
smell — so good, indeed, that it is the guiding sense, instead of vision.

A great many surmises have been made as to the function of the
pecten, the first of them not many years after its discovery in 1676.
Nearly all its students agree that it must nourish the interior of the eye;
but its peculiar form, and particularly the great variations in its form

*This superorder includes all living birds excepting the ostrich-like forms and tinamous
(superorder Palaeognathae) and the likewise primitive penguins (superorder Impennes).

tFor comparison, note the eye of a turkey, shown at natural size in Figure 142a and b,
p. 420.

THE PECTEN AND ITS ANALOGUES 651

and size, have made it seem unlikely, to most, that nutrition is its chief
purpose. So, a great deal of thought has been spent upon its interpre-
tation. One of the most recent and interesting theories has been dis-
cussed on pp. 365-7. It has been variously held to cast a shadow on the
retina, or not to do so; and the supposed shadow has been involved by
one investigator in movement-perception, and by others in the pre-
vention of monocular diplopia during binocular vision, or in the sup-
pression of the binocular field during monocular fixation. It has even
been considered to serve as a 'dark mirror', transforming a too-bright
image (cast upon it by the lens) into a comfortably-bright one (relayed
from it to the retina), and making it possible for a ground-feeding bird
to see an approaching hawk in the sky without looking upward. The
pecten has been believed to adjust intra-ocular pressure (by swelling and
shrinking) during accommodation or during changes in the altitude of
flight, to serve as a proprioceptive sense-organ for the regulation of
accommodation, or even to assist mechanically or hydraulically in the
deformation or displacement of the lens. It has been held to be primarily
a heat-radiator, of especially great value to arctic, alpine, and high-flying
birds. To it has been ascribed a function similar to that of the holostean-
teleostean chorioid 'gland' — the smoothing out of intra-ocular blood-
pulsations, analogous to the action of an air-chamber on a reciprocating
pump.

To each of these theories so many objections stand in the literature
that we shall not consider them in detail here. Suffice it to say that it is
unlikely that the pecten casts a shadow outside of its own base — or casts
one where it would do any good; that its shape, volume, and position
have not been found to alter during accommodation; that its size does
not correlate with the coldness of the air to which its owner exposes
itself; that it could not conceivably reflect an image even as good as
those one sees in fun-house mirrors; and that no sensory netve fibers or
endings have ever been demonstrated in it. We can cling, however, to
the demonstrations by Abelsdorff and Wessely of a ready diffusibility
of blood solutes through the walls of its vessels (despite their peculiar
and thick hyaline coats) into the vitreous, and of its capacity for com-
pensatory hypertrophy following the surgical excision of the ciliary
processes.

It is because the writer does not believe that the pecten has any
'ulterior' function — particularly, any function with a directive connec-
tion with the relationship of the eye to the environment— that the struc-

652 BIRDS

ture has found no great place in the ecological Part of this book. We
shall find reason to consider the pecten related to the habits, particularly
the visual habits, of birds; but it is the habits which have molded the
pecten, not the pecten which brings about the habits. To obtain a proper
perspective on the intriguing variations of the pecten, it will be necessary
to make an apparent digression and consider the whole comparative pic-
ture of which the pecten is but one detail :

In the first place, it must be borne in mind that the only fast-living
tissue in the whole posterior segment of the vertebrate eye is the sensory
retina. The one richly vascular structure universally present is the chor-
ioid coat; but all the blood-filled tubing of the chorioid exists simply in
order to maintain a rich flow in the choriocapillaris; and the latter exists
solely to nourish the retina — with special reference to the greedy rod-
and-cone layer. If the requirements of the visual cells are not too high,
there may be enough pabulum left in the trans-retinal exudate of the
choriocapillaris to care adequately for the needs of the inner layers of
the retina. We should expect this to be the case, ceteris paribus, when
the rods are abundant and the more highly metabolic cones are absent
or present only in reasonable numbers. But if the chorioid of a partic-
ular eye cannot supply a cone-rich visual-cell population in an extensive
retina, and the neuronic layers of that retina as well, then we may expect
to find some additional vascular device, advantageously situated to
supply the inner reaches of the retinal tissue. Ciliary processes, when
present, are not so situated; for they lie too far anterior to the main
mass of the retina, and their secretion (the aqueous humor) passes
too largely and directly into the anterior chamber and is too promptly
drained therefrom.

We found no supplemental nutritive device (hereinafter to be abbre-
viated as 's N d') in the lampreys. These forms have small eyes, but
most have many cones and tend toward diurnality. Their eyes are per-
haps simply too primitive to have achieved physiological perfection.

The absence of any s N d in the elasmobranchs is readily understood
in view of their nocturnality and their pure-rod retinae.* Nor should the
modern chondrosteans require anything more than their chorioids. In
the holosteans and teleosts, however, we have essentially arhythmic and
bright-light groups, and we note that these fishes are all provided either

* Mere habitual exposure, as such, to strong light — apart from an accompanying high cone: rod
ratio — may tend to demand an s N d; it does not seem to have occurred to physiologists
that a bright, minified miage will inevitably warm the retina and quicken its metabolism.

THE PECTEN AND ITS ANALOGUES 653

with a network* of 'hyaloid' vessels at the vireo-retinal interface, or with
a falciform process — an obvious physiological counterpart of the avian
pecten (the pecten being essentially an ectodermal imitation of the older
structure!). It is not too much to hope that someone will sometime
determine whether the retinae of the hyaloid-vessel teleosts have greater
requirements of glucose and oxygen than those of the falciform-process
species. The retention of one S N D or the other in even the most strongly
nocturnal teleosts may seem disturbing to our thesis; but their nocturn-
alities are probably all secondary, and there has been no such urgent
need to eliminate an S N D from a secondarily nocturnal eye as to evolve
one in a secondarily diurnal one. The presence of vitreal vessels in
Polypterus, Protopterus, and Lepidosiren may have such an explanation.

Among the anuran amphibians, the ranid frogs alone exhibit the
primitive arhythmic or diurnal habit of the group, as is evidenced by the
persistence of yellow cone oil-droplets in those forms alone. All known
anurans have vitreal vessels, whose presence (in as full development?)
in the secondarily nocturnal toads and tree-frogs is thus a failure-to-
discard. It is only natural that the urodeles and cxcilians have never
developed such vessels.

Turning to the reptiles, we are confronted by the paradox that neither
the diurnal turtles nor the nocturnal crocodilians have preserved the
ancestral conus papillaris in a useful condition. Its loss in the croco-
dilians (and in Sphenodon) makes good sense; but the turtles all have
many cones — some, perhaps, only cones — in their retinae. The turtle
rates as 'sluggish' alongside the average lizard. The latter has the conus,
of course ; and it would be interesting to know whether the requirements
of the relatively crude (though cone-rich) turtle retina are sufficiently
lower than those of lizard retinze to explain the difference with regard to
the conus. Again, among the lizards themselves, the relative size of the
conus does not go perfectly with diurnality-versus-nocturnality : it is
smallest in certain geckoes and other nocturnal lizards (Pygopus, etc,) ;
but there are geckoes with large coni, and the chameleons have very
small ones. Anyone who has ever watched the 'slow-motion' performance
of a true chameleon, however, should be willing to imagine that its
retinal metabolism may be little if any higher than that of a tortoise.
As for the geckoes, there are reasons for thinking that their peculiarly
pure-rod retinae have a physiology much like that of a pure-cone one.

* Richer in Lepisoiteus than in Amij, according to Virchow.

654 BIRDS

In the snakes, we have a pretty analogy for the situation in the tele-
osts, for here a mesodermal vascular papilla has been given a trial, and
practically abandoned in favor of a vitreal-vessel system (the latter pre-
sumably more efficient, since it is in so immediate contact with the tissue
which it serves). The retinal plexus does not seem to have reached a
high state of development in the Boidse (which are nocturnal), but it
has full expression in the Colubridae, where the total area of its vessels
is said to equal one-third of the whole area of the retina; and it has
persisted unchanged in the higher families despite their wholesale re-
versions to nocturnality — perhaps because the ophidian chorioid had
become so very thin, so that it was as easy to keep the hyaloid vessels as
to discard them and rebuild the chorioid (cf. Protopterus!) .

To anticipate the next Chapter : the mammals characteristically have
many vessels and capillaries embedded in the inner layers of the retina.
This greater intimacy of relationship, as compared with the fish-anuran-
snake situation, is only to be expected since the mammals are warm-
blooded and those other groups are not. Just so, the buttressing or
pleating of the avian pecten (often claimed to promote structural
rigidity, which of course it incidentally does) is a secretory-surface-
increasing device which these hot-blooded creatures require, in contrast
to the lizards and the extinct reptiles which really evolved the lizard
conus. A vestigial conus occurs in many of the lower mammals, partic-
ularly in marsupials and rodents. The retinal vessels are lacking in the
monotremes, and are lacking or greatly reduced in many other nocturnal
mammals. They are best developed in the (diurnal) primates and in the
(arhythmic) ungulates and carnivores. Where, as occasionally, the
retinal vessels extend out to the outer nuclear layer as if to supply even
the visual cells themselves, it is in forms whose chorioids are exception-
ally under-developed (dormice, flying-squirrels) or are insulated from
the visual cells by a relatively impermeable retinal tapetum (opossum;
the retinal tapetum of the crocodilians also seems to interfere, for the
chorioid is extra-thick behind it — p. 613). It is a toss-up whether the
embedded retinal-vessel system of mammals, or the pecten of the birds,
is 'better'. The retinal vessels are a more direct means of supplying the
retina; but the pecten perhaps interferes less with vision — the mam-
malian retinal vessels have always to be excluded from the vicinity of a
fovea.

The whole s N d picture thus reveals a rather consistent relationship
with habits which would seem to carry with them a high level of retinal

THE PECTEN AND ITS ANALOGUES 655

metabolism, such that the chorioid is unable to take care of the whole
thickness of the retina — occasionally, unable to supply even the whole
requirement of the visual cells alone. We can now again approach the
avian pecten, prepared to inquire more astutely whether its variations
really demand explanation other than the one which seems to cover the
supplemental nutritional structures of other vertebrates.

A large amount of information on the size of the pecten in different
birds has been gathered together by Kajikawa and Franz. It is not easy
to interpret the data, for as often as not only the number of folds of the
pecten has been recorded. This value is however as useful as any other
single one; for even if we knew the length, width, and height of a pecten,
and its total surface area, we should still need to know its total blood-
vessel area, blood capacity and rate of flow, the area and volume of the
retina and its rate of oxygen- and glucose-consumption, before we could
compute any very precise ratios as a basis for the comparison of one eye
with another. Not all of these facts are known for any one bird, let alone
for an assortment of birds with various habits.

In a great majority of birds, the Jength of the base of the pecten is
about equal to half the horizontal diameter of the eye, and the number
of folds in the pecten runs high — about 14-27, with 30 as the maximum
(in Garrulus glandarius) . In this category are most of the ground-
feeding, gallinaceous birds and the perching birds (Order Passeriformes,
comprising about half of the 20-odd thousands of kinds of birds) , These,
and indeed most other birds, feed upon small objects and have high
capacity for resolution and accommodation in proportion to the size of
their eyes. Still greater ranges of accommodation are found in the
largest-eyed predaceous birds, the hawks and eagles. In these birds the
volume occupied by the pecten is relatively about as large as in most
passerines, but the folds are coarser and consequently somewhat fewer
(mostly 13-17). The owls and swifts are known to accommodate but
little. Owls have only 5-8 pecten folds, and the number in Apus apus
(11) is just low enough to call 'low'.

These generalizations have been known for some years, and have led
many investigators to agree with a theory of Rabl, which he based upon
correlations of the number of pecten folds with the relative size of the
ringwulst (which, as we have seen, is essentially involved in sauropsidan
accommodation) . Rabl held that since the degree of development of the
pecten goes with the degree of development of the accommodatory
mechanism, the pecten must be a part of that mechanism.

656 BIRDS

This correlation with accommodation still stands despite all the
evidence, experimental and otherwise, that the pecten has nothing to do
with accommodation. If the relation of the two is not causal, then we
must look for a third correlate which ties the first two together. This
appears to be furnished by the retinal metabolic rates of the birds :

If, as the comparative s N d situation suggests, the retinae in actively
diurnal vertebrates, with relatively high visual acuities, consequent high
cone: rod ratios, and good accommodation, have higher metabolic re-
quirements than the rod-rich retinae of nocturnal, crude-visioned, poorly-
or non-accommodating forms, then of course we should expect the avian
pecten to 'go with' accommodation; but it is really going with diumality,
high visual acuity, and bustling activity.

Reviewed with this thesis in mind, most birds do seem to have either
large and many-folded pectens, or small ones, depending upon their
behavior toward illumination and their general level of activity. In noc-
turnal birds, the length of the base of the pecten is decidedly less than
half the eyeball diameter. Among the palaeognaths* the ostrich and rhea
are bold, light-loving creatures and have up to 25 or 30 pecten vanes.
The cassowary is shy and crepuscular, spending most of its time in the
densest forests, and has a small pecten with only 4-5 folds. Moreover,
the cassowary pecten appears degenerate in that it has been invaded by
mesodermal connective tissue. The lizard-like pecten of the strongly
nocturnal Apteryx has no vanes at all, whereas those of some lizards
have three or four.

It has been shown that the pecten of a large owl {Bubo bubo) is
smaller than that of an eagle (Aquila chrysa'etos) having the same retinal
area. Smaller owls compare in this same way with hawks; and the pecten
in all owls is incomplete in that it lacks a 'bridge'. The nocturnal frog-
mouths (Podargus spp.), close relatives of the owls, have bridgeless
pectens which are relatively even smaller, with but three or four folds.
The European goatsucker Caprimulgus europceus, another nocturnal
owl-relative, has three to five pecten folds.

Among ducks and geese, which mostly have 10-16 folds, a conspic-
uous form with its six folds is the peculiar Cereopsis, a goose which
seldom leaves the ground (and, incidentally, has practically no ring-
wulst). The nightingale, Luscinia megarhyncha, has been claimed to
have only five folds; but this is an old and doubtful record. The parrots

*Whose radiate pectens should probably be considered separately until we know more
about their relationship to the undulant pectens of other birds.

THE PECTEN AND ITS ANALOGUES 657

have rather low fold numbers — 7-14. This is hard to explain away, for
most parrots are active diurnal birds and fly a good deal. They would
seem not to have high visual-acuity requirements, however; for, with the
exception of the notorious sheep-killing (?) kea, they restrict themselves
more to gross vegetable food than do any other birds. The eyes of parrots
bear other surprises, and would be well worth intensive study : they have
the narrowest known binocular fields (p. 295), and lack the customary
red oil-droplets (pp. 499-500). It can be said, though, that within the
parrot group the number of pecten folds varies as one might expect, for
the nocturnal owl-parrot (Strigops habroptilus) has only four to six folds.

Rather low numbers (i.e., less than 12) occur in many sea-birds, shore-
birds, herons etc. Some of these are nocturnal, others not. One clear-cut
example of correlation — which could be multiplied — is the stone-curlew
(Burhinus cedicnemus) , which feeds only at night, has very large eyes,
and has only eight pecten folds.

The general correlation of large, elaborate pectens with diurnality and
of reduced folds with nocturnality was noticed by Wagner back in 1837.
This was thirty years before the formulation of the Duplicity Theory;
and it was only long after 1867 that it was first realized that cones and
rods might have very different metabolic rates and requirements. Wag-
ner studied 108 species of birds, and though all the additional species
examined since have only borne him out, his idea has been quite ignored
or forgotten since the turn of the century when Virchow last accorded
it a few words in print. Jokl did not know of it when, in 1923, he per-
ceived the physiological interchangeability of the various S N d's — but
thought that the metabolic level of a retina, determining the need or
dispensability of an s N D, was governed by the activeness of the animal.
Thus, he explained the absence of a conus in both turtles and croco-
dilians on the basis of sluggishness (forgetting Sphenodon, which also
lacks a conus and is sluggish as well as nocturnal) , and he accounted for
the reduced pectens of Apteryx, Casuarius, and Struthio {sic) on anal-
ogous grounds — i.e. flightlessness. The ostrich has plenty of 'folds'; and,
though flightless, it is very far from sluggish.

Wagner and Jokl were each on one rail of the right track. From all
present indications it does not appear that we need ascribe to the pecten
any 'intentional' activity other than the giving off of nutrients for the
retina to absorb from the vitreous. That it gives off heat (which however
is not needed) goes without saying. That considerable water escapes
from it also is clear from certain of Abelsdorff and Wessely's experi-

658 BIRDS

ments; but this serves only to provide water which, in a pectenless eye,
the vitreous would get from the ciliary epithelium anyway. The need for
a pecten (or for any other s N d) , and for a large one or a small, seems
to depend solely upon the rate-of-living of the sensory retina. Some of
the factors, at least, which heighten this rate are diumality, activity, and
high retinal temperature (owed chiefly to warm-bloodedness, but assisted
by the absorption of photopic images in the contiguous pigments) . Con-
versely, it is depressed by the elimination of cones in nocturnality, by
sluggishness, and by low retinal temperature.

The interplay of these factors is various. Probably the turtle, though
diurnal, needs no conus because it is sluggish. Probably the large geckoes,
though nocturnal, need one because they are extraordinarily active. Prob-
ably the chameleon's conus is tiny because the animal, though diurnal, is
sloth-like in all its movements except the extension of its fly-catching
tongue. Probably the flying-squirrel, though nocturnal, needs retinal
capillaries because it is active and warm-blooded. But these are guesses —
we have no cold figures on the retinal metabolism of these forms, and of
their close relatives which have different habits and different S N D con-
ditions.

Before any final ballot is taken on the prosaic theory offered here in
explanation of the S N D, in general, and the many more glamorous and
intrinsically more 'attractive' interpretations of the pecten, we need very
badly to know more about the true sizes of pectens — the area over which
they expose the blood circulating in them, the rate at which the blood is
changed for fresh, the permeability of their vessels, and so on. Then,
such data must be compounded with the status of the chorioid, with the
area, thickness, and histology of the retina, and with the results of in
vitro determinations of the metabolism of unit pieces of retinal tissue
from various birds and various other vertebrates, wisely selected in the
light of the whole S N D situation.

These are problems for a physiologist to attack : he has the apparatus
and the methods*; and he can be assured in advance that his findings
will be of great value in themselves even if they do not yield correlations
which take the mystery out of the pecten. To date, ornithologists and
ophthalmologists have been too content to sit back and speculate about
the pecten, though they were told by von Husen, back in 1913, that only
physiological experimentation would reveal the whole meaning of the
structure. As Mark Twain said of the weather, everyone talks about the

*See, for example, the paper of Lindeman (1940).

THE AVIAN RETINA 659

pecten but no one does anything about it. The above discussion commits
this same crime, but offers a reasonable working hypothesis which, it is
hoped, will receive a proper test at the hands of experimental biologists.

The Retina — The precision and elaboration of retinal layering reaches
its peak in the birds. Scarcely a cell is out of place — i.e., in a layer
inappropriate to its type; and the inner nuclear and inner plexiform
layers are more clearly differentiated into sub-layers than in other verte-
brates with the possible exception of the prairie-dog. The fovea of the
birds is the most perfect of all foveae, and many birds have more than
one in each retina.

The cells of the pigment epithelium are of the usual sauropsidan type,
with numbers of fine processes, each containing a chain of bacilloid
fuscin granules and extending as far as the inner segments of the visual
cells. The latter are so slender and so tightly packed, and the ratio of
conductive to sensory cells is so high, that all three of the nuclear layers
and the inner plexiform as well (but not the outer) are relatively thick.
The whole retina (whether diurnal or nocturnal) is thereby thickened —
one and one-half to two times as thick as in vertebrates in general, and
equalled only in some of the teleost fishes (compare Fig. 193a with Fig.
19, p. 43; note also Fig. 72, p. 177). Some sample nuclear-layer counts,
made in the general fundus (away from the influence of any fovea
present) , follow : Ro^,s ^p .

Species: Outer Inner Ganglion

nuclei nuclei cells

Week-old chick iGallusdomesticus) 2.5 18 2.5

Domestic pigeon (Co/m 772 ^d /m'd) 3 15 2

Robin (Turdus migratorius) 3 28 3

English 'sparrow^ {Passer domesticus) 3 12 2

Flicker (Coldptes auratus) 2.5 18 2

Marshhawk {Circus hudsonius) 4 20 3

Red-tailed hawk {Buteo borealis) 3 17 2

The inner nuclear layer contains the bodies of many amacrine cells of
several types, as well as a greater number of bipolars. The nuclei of the
Muller fibers are much elongated in the direction of the retina's thick-
ness, and form a single compact layer, within the inner nuclear layer,
about one-half to three-fifths of the way through its thickness from the
outer to the inner side. Outwardly from this line of Muller nuclei (to-
ward the outer nuclear layer) are the bodies of the bipolars. Inwardly
(toward the ganglion layer) lie those of the amacrines.

660

BIRDS

In the inner plexiform layer a variable number of faint bands can
always be seen, running parallel to the retinal surfaces. These mark the
distinct levels at which the various types
of amacrines expand their terminal ar-
borizations. At these same levels, for the
obvious purpose of binding together the
synapses at each level, there are vari-
cosities on the filaments of the Miiller
fibers. These cells are very different from
those of other retinae, for in their course
through the inner half of the retina they
depart from the usual sponge-like struc-
ture, and each cell breaks up into a great

Fig. 193 — The avian retina and its visual cells.

a, portion of fundal retina of week-old chick. x500.
p- pigment epithelium; v- visual cells; o- outer nu-
clear layer; b- bipolar elements of inner nuclear
layer; m- row of Miiller-fiber nuclei; a- amacrine
elements of inner nuclear layer; /'- inner plexiform
layer (note stratification); g- ganglion-cell layer;
n- nerve-fiber layer.

b, peripheral single cone and double cone, periph-
eral and fundal rods, of Passer Jomesticus. x 1000.
p- paraboloid.

THE AVIAN RETINA 661

number of parallel threads, which terminate in an infinity of tiny trump-
ets to compose the tile-work of the internal limiting membrane.

The diurnal majority of birds have great numbers of single and double
cones (their oil-droplets of divers colors, as in turtles) , and relatively few
rods. The rods may be restricted to the periphery or may even be entirely
lacking in some instances. In nocturnal birds the rods predominate,
though there may be large numbers of cones as well, some of them with
pallid, though definitely pigmented, oil-droplets. The rod and cone
nuclei and foot-pieces are of the same, 'cone', type in diurnal birds, but
are differentiated in many or all nocturnal birds, as they are in other
duplex vertebrates whose rods are numerous and very slender (teleosts,
mammals) . The rods of all birds contain rhodopsin.

These visual-cell types are pictured in Figure 193b (in their plump,
easily-studied peripheral versions — compare Fig. 22e, p. 54) . The avian
cones are the same elements, phylogenetically, as their opposite numbers
in the reptiles and the lower mammals (see Plate I). The bird rod has
a paraboloid like those of chelonian and crocodilian rods, though it may
be difficult to make out in the slenderized rods of the fundus, where it
appears to form a long, slender tube. The rod is clearly comparable with
the rod of the turtle, that of the alligator, and the cone of Sphenodon
(see Figs. 176b, 177a, 179; pp. 612, 615, 621) ; but it has become a rod
independently in the birds (or perhaps in their immediate ancestors —
see Plate I), and is fully differentiated in the morphological sense only
in nocturnal birds (v.s.).

The proverbial resolving power of the bird eye is based partly upon
its large size and the relatively large image cast upon the retina, partly
upon the dense concentration of the cones and the high ratio of optic-
nerve fibers to visual cells. In the little white wagtail (Motacilla alba),
outside the foveal region, Franz found approximately 120,000 visual
cells and 100,000 ganglion cells per square millimeter of retina (compare
the human fovea: 200,000—200,000). In an owl (Bubo bubo), with its
relatively great summation, the corresponding figures were 56,000 and
3,600 (compare the overall summation-ratio of the human retina: ca.
125:1). In the fovea, even such birds as little Passer domesticus have
400,000 or more cones per square millimeter — and each cone presumably
has its own bipolar and ganglion cells. The grand champion of all
foveae is perhaps that of a hawk (Buteo buteo) , in which Rochon-Du-
vigneaud found 1 ,000,000 cones per square millimeter. Even outside the

662 BIRDS

fovea this hawk, with its approximately man-sized eye, has nearly twice
the resolving power of human foveal vision; and, foveally, the visual
acuity of some hawks and eagles reaches a value at least eight times
that of man.

Chapter 18
MAMMALS

See also pages:

6-22 structure of human eye

26-8 refractive errors

29-36, 247-53 human dioptrics, accom-
modation

47 Fig. 21a

49-50 horizontal cells, amacrines

50-1 retinal nutrition

51-2 optic nerve, chiasma

56-60, 166, 176-7, 215-7 visual cells

67 human retinal summation

74-103, 168, 194, 198, 207, 211-2, 215-6,
245-6 vision

81-103, 333-8, 462-72, 504-23 color vision

104-17 embryology

134-5, 138-9 relationships

143, 191-6, 199-201, 203-5 yellow mtra-
ocular filters

145, 164, 169, 170-1, 203-5, 208-9, 210
habits

150, 166 photomechanical changes

153-8, 162-3, 218-21, 227-8 pupil

171-5 non-retinal acuity adaptations

178-80, 367 blind spot

181-3, 187-8, 190, 311-2 area centralis,
fovea

210-4 non-retinal sensitivity adaptations

213 tubular eyes

228-35, 238-46 tapeta, eyeshine

247-57, 283-8, 444-8 reraction, accommo-
dation

285-6 ciliary body

289-92, 296-300 visual fields

300-3, 310-2 eye movements

313-38, 341 stereopsis

334-8 central visual pathways

339 Fig. 124

340 median eye

342-65 movement perception
442-8 amphibious adaptations
523-4 dermal color changes
543-51 coloration of eye

The Class Mammalia contains three major divisions which are not
serially related, but represent three branches from a single stem. The
lowest mammals, closest to the reptiles, are the monotremes. These egg-
laying forms include only the duck-bill or platypus (Ornithorhynchus)
and the echidnas or 'spiny ant-eaters' (Tachyglossus and ^aglossus
[= Echidna and Proechidna] ) . Ranking higher in point of specialization
and anatomical distinctness from the reptiles, but not derived directly
from monotremes like those now living, are the marsupials. These like-
wise have yolky eggs, but hatch them inside the body and bear the young
alive in an embryonic condition. The young complete their development
on a milk diet, outside the mother but usually inside an abdominal
pouch. In the common opossum, Didelphis virginictna, the 'embryology'
of the eye continues for 30-40 days after birth. The highest (placental)
mammals nourish their young inside the mother's body by means of a
'placenta'. They were not derived from marsupials, but with them, as
one of two branches.

663

664 MAMMALS

(A) MONOTREMES AND MARSUPIALS

In these 'lower' mammals the eye alone would prove the reptilian
origin of the whole mammalian class. Indeed, with the exception of
exactly two features — one of them outside the eyeball (in the oculo-
rotatory musculature) and the other one inside (in the ciliary body) —
the monotreme eye is so completely reptilian that it affords no am-
munition for use against those few mammalogists who claim separate
reptilian origins for the monotremes and for all other mammals.

The marsupials originated as opossum-like animals, and only such
forms (together with Ccenolestes) have been able to survive in the
American home of the group. In Australia however, where they became
isolated from placental flesh-eaters, the marsupials differentiated into
a number of types, many of them imitative of placental types. Thus,
there are marsupial mice, rats, marmots, rabbits, flying-squirrels,* jer-
boas, bears, cats, wolves, ant-eaters, and golden moles. There was once
even a marsupial 'lion', though it was probably a mild-mannered vege-
tarian. The marsupials have avoided the water, so there are no marsupial
seals or porpoises — the tropical American water-opossum, Chironectes,
is the only aquatic marsupial. Nor have the marsupials developed any
hoofed types; but the larger kangaroos fill about the same ecological
niche.

The lower marsupials are mostly carnivorous and the higher types
(phalangers, kangaroos) herbivorous. Most marsupials, like the mono-
tremes, are crepuscular or nocturnal to some degree; but the larger
kangaroos are arhythmic and a few are quite strongly diurnal. In keep-
ing with the adaptive radiation of the marsupials, their eyes show great
differences from form to form. In proportion to the number of species,
they have had woefully little attention as compared with the placentals.
The marsupials are really the central group of mammals, and deserve
much more thorough exploration, from all biological viewpoints, than
they have ever yet received.

The Monotreme Eye — The eye of Ornithorhynchus has been de-
scribed only once, by Gunn in 1884 from material preserved in whisky
by a Mr. Sinclair, who clearly took his science very seriously. The eyes
of the two genera of echidnas have been described by Franz, by Kolmer,

*A fascinating coincidence is that the flying-squirrel type has been evolved more than once
in the rodents — by the true flying-squirrels and in the Anomalurid»- — and more than once
also in the marsupials: there are three kinds of flying phalangers, each a close relative of a
different non-flying form.

THE MONOTREME EYE 665

and by Gresser and Noback. None of these accounts is entirely accurate
— all incorporate particularly serious errors in regard to the shape of the
globe (which is 'avian' only when collapsed) and the presence of a
ciliary muscle (which is wholly lacking, though two of these authors
describe it as having the same three types of fibers — meridional, 'radial',
and circular — as the ciliary muscle of man). The ensuing descriptions
are based upon preparations of Tachyglossus and Ornithorhynchus made
by Kevin O'Day, and upon correspondence with him. Statements of
earlier workers which happen not to be refuted by O'Day's splendid
material are also incorporated.*

Ornithorhynchus has an excellent nictitating membrane. Tachyglossus
has none; but both genera have retractor bulbi muscles. The lids are
plump and small in both, and in Tachyglossus are closed by swinging
rather than by sliding. Small Meibomian glands, still with relation to
hair follicles, are present in Ornithorhynchus. These may be orimentary
(see p. 40) ; but the same situation occurs in one placental, the hedge-
hog (Erinaceus) . They are lacking in Tachyglossus and Zaglossus. Like
most Sauropsida, Tachyglossus has a tarsus in the lower lid only, while
Ornithorhynchus has one in each lid. Both genera are supposed to have
both lacrimal and Harderian glands (but Kolmer found only serous
glandular tissue in Zaglossus) . The adnexa in Ornithorhynchus thus
show no specialization for the amphibious life of the animal. In fact,
those of the echidnas exhibit rather more reduction, which seems largely
explained by the presence in those forms of a keratinization of the
corneal epithelium, no doubt in adaptation to the ant-eating habit (as
in armadillos and aard-varks) .

In the arrangement of the superior oblique muscle, the monotremes
are wholly 'mammalian'. In the echidnas there is a slip which runs from
the old sub-mammalian origin (on the anterior nasal orbital wall) to
an insertion on the globe; but merging in this same insertion is a second
slip, muscular almost to the globe, which comes through a pulley from
an origin only a few millimeters anterior to the deep point-of-origin of
the four recti. The duck-bill has only this long portion, and moreover
has it as in higher mammals, /'. e. originating with the recti and becoming

*Dr. O'Day has been trying for several years to find time to prepare a monograph on the
eyes of the monotremes. When this does finally appear it will greatly extend, and no doubt
partially contradict, the present treatment. In the meantime, because of the slowness and
uncertainty of communication with Australia, the writer has made bold to discuss O'Day's
findings without seeking his permission — they seem much too important to be left out of
this book.

666 MAMMALS

tendinous before reaching the pulley, with the latter chondroid rather
than soft as in the echidnas. This seems too strong a similarity to the
higher mammals to be dismissed as a coincidence by those who consider
the monotremes to have originated from a separate reptilian stock. It is
not certain what called forth the elongation of the mammalian superior
oblique. Such an elongation may have occurred twice. In this connection,
it would be nice to know whether the optic chiasmata of the mono-
tremes are only partially decussated. Both types have wide binocular
fields, that of the echidnas being projected forward and that of the duck-
bill largely upward.

The eyeball is usually figured with a short axis and a pronounced
circumcorneal scleral sulcus, both of which are collapse-artefacts. Cor-
respondingly, its shape has most often been called 'avian',* Actually,
the eyeball is everywhere convex and is spherical in all monotremes. This
sphericity, so reminiscent of the snakes, has the same basis — a total
disappearance of the ancestral scleral ossicles (Fig. 194a) .

The eyeball of Tachyglossus is eight or nine millimeters in diameter,
that of Ornithorhynchus about six. In all monotremes the sclera con-
tains the cartilage cup with which we have become so familiar in pre-
ceding chapters. In Tachyglossus the cartilage is 27[J, thick in the region
of the optic nerve, 14[X thick near its sharp anterior lip. In Z.aglossus
(a larger animal) it averages 160|i in thickness. In the duck-bill it is
even thicker fundally (400(l) but tapers to 25 (X near its knife-edge
termination. The cartilage reaches to the posterior ends of the ciliary
processes in Ornithorhynchus, but stops opposite the ora terminalis in
Z.ctglossus and a little behind the ora in Tachyglossus. An outer layer
of fibrous scleral tissue about equal in thickness to the cartilage (but
only 96 [A in ^aglossus) , continues forward (receiving an addition which
replaces the cartilage) through a zone formerly occupied by the scleral
ossicles, and blends with the substantia propria of the cornea. In Tachy-
glossus at least, an outer fraction of the substantia propria is easily seen
to be continuous with the conjunctival corium or 'episcleral' connective
tissue. A loose layer of episcleral blood vessels, from which capillaries

*And all the sauropsidoid internal features are likewise called avian by those who are
familiar with their occurrence in birds but ignorant of their occurrence also in the reptiles.
Attempts to derive the monotreme eye from the avian, and coy insinuations that the two
eyes are identical through convergence (justifying the 'bill', webbed feet, spurs, and egg-
laying habit of the platypus), are naive in the extreme; but they continue to be made.

The astute Franz indicates in several places that he suspects that the 'avian' form of the
usual preserved echidna eye is a result of collapse. O'Day finds that this collapse occurs
very readily in both Tachyglossus and Ornithorhynchus.

THE MONOTREME EYE

667

are sent into the cornea for some distance, marks the boundary. No-
where else above the teleosts is it so readily to be seen that an outer
portion of the substantia propria is homologous with the dermis rather
than with the dura (Fig. 194a; cf. Fig, 151, p. 451). A Bowman's mem-
brane has been claimed for Ornithorbynchus, but none can be made out
in Tachyglossus. Both these genera have the usual Descemet's layers,
but Kolmer could not make out the elastic membrane in Zaglossus.

Fig. 194 — The monotreme eye.

a, sertion of eye of Tachyglossus sp. x8. Drawn from a preparation of O'Day.

b, inner surface of segment of anterior uvea of Tachyglossus. After Franz.

av- anterior surface of vitreous; cd- conjunctival dermis; ch- chorioid; cp- ciliary process;
cs- canal of Schlemm; cw- ciliary web; ev- episcleral vessels, marking boundary between
dermis and fibrous tunic; »'- iris; /, /- external limits of cornea; m, m- rectus muscles;
ot,ot- ora tertninalis retina; r- retina; s- sphincter; sc- scleral cartilage (black); s\- fibrous
layer of sclera; ^- zonule (main portion).

In keeping with its aquatic habits the duck-bill has a relatively broader
cornea than Tachyglossus, but it has a deeper anterior chamber (cornea
4.0mm. in diameter in a 6.0mm. eye, vs. 3.4mm. in a 8.0mm. eye; cham-
ber 1.25mm. deep ys. 0.9mm.). The duck-bill's corneal substantia propria
is only one-fourth as thick as the echidna's, but its epithelium is much
thicker and nearly equals the propria — such thickening being highly
characteristic of aquatic vertebrates in general. The duck-bill cornea is
lOOfl thick peripherally, only 55 [i apically. Zaglossus reverses this rela-

668 MAMMALS

tionship, with its whole cornea 320[X thick centrally (with 264^, of
propria) and 540[1 peripherally (460[X of propria). Comparable figures
for Tachyglossus are 350-290, 330-210.

The chorioid is only 50[X thick in the duck-bill, a little more than
twice this thick in Tachyglossus. Histologically, it is ambiguous — as
turtle-like as it is 'mammalian'. The pigmented, laminated suprachori-
oidal layer or 'lamina fusca' is conspicuous, as is the choriocapillaris,
whose elements are unusually large in lumen and are readily seen to be
connected with the large veins.

In all three genera the iris is most simple, its web consisting of little
more than the two heavily pigmented retinal layers and a few small
blood vessels attached loosely to the anterior face. There is no dilatator,
but there is a massive sphincter around which the pigmented retinal
layers are rolled so that their mutual edge lies on the anterior face of
the iris. The root of the iris lies opposite the limbus in the duck-bill, but
well back of this landmark in the echidnas. There is no pectinate liga-
ment; but, as in reptiles which lack one, there is a thin anterior contin-
uation, past the iris root, of ciliary-body connective tissue, which is
adherent to the inner surface of the fibrous tunic and tapers to a knife-
edge aligned with the peripheral margins of the Descemet's layers. The
canal of Schlemm is embedded in this uveal meshwork tissue, as it is
in sauropsidans in general. The iris is dark brown in life, the pupil
always circular.

TThe anterior continuation x»f the chorioid forming the uveal portion
of the ciliary body is thin, only lightly pigmented, and not sharply de-
marcated from the inner layers of scleral fibers except where it underlies
the tallest portions of the ciliary processes. There is no trace of a ciliary
muscle, and the writer is quite unable to imagine what it may be that
others have mistaken for one. The ciliary processes are low, puffy, and
tortuous, and number about 60 in Tachyglossus. Their anterior ends are
interconnected by an annular shelf-like structure — like a miniature iris —
the 'sims'. This German term has never been translated; perhaps it is
high time that it was. Since the sims connects the ciliary processes, which
give the ciliary body its name (cilia = hairs or threads) , after the fashion
of the webbing which connects the toes of a duck or a frog, it will be
called here the 'ciliary web' (Fig. 194b, cw).

The ciliary web is a decidedly mammalian character, shared by many
marsupials and placentals but by no sauropsidans. Every other feature
of the monotreme eyeball — whether the feature is a structure, or the

THE MONOTREME EYE 669

absence of a structure — occurs in some living reptilian group. The ciliary
web alone* thus keeps the eye of the monotreme from being entirely
reptilian, with its closest morphological resemblance to the eye of the
likewise-nocturnal crocodilian.

The lens is unexpectedly small, flat, and anterior in position. The
topography of the monotreme anterior segment, particularly in the
echidnas, is in fact not at all sauropsidan but more like that of the
sirenians and primates. Tachyglossus has the flattest of all lenses, with
a flatness-index (diameter divided by thickness) of 2.75.+ This value is
closely approximated elsewhere only in some of the higher primates,
including man (ca. 2.7). At its equator, the lens epithelium is twice
as tall as at the anterior pole, constituting perhaps a vestigial ringwulst.
A similar situation obtains in the duck-bill, and also in some marsupials.
The lens of the duck-bill, in keeping with the aquatic habit, is much less
flat— 2.66/1.93 = 1.38 (Kahmann), 2.45/1-75 = 1.4 (Gunn), or 1.5
(from a photograph of O'Day's — scale not given) . O'Day compares its
form with that of the lens of the local Murray turtle, Chelodina longi-
collis.

No monotreme has any demonstrable accommodation, and there are
no reports as to refractive conditions. It is not known whether Ornitho-
rbynchus approaches emmetropia in either air or water, but the impli-
cations are that the eye is better adjusted to the latter medium. The
echidna eye looks as though it must be extremely hypermetropic; but
only a study of the living animal can settle the matter.

In both Ornithorhynchus and Tachyglossus the numerous zonule
fibers arise from the coronal zone of the ciliary body and from the free
portions of the ciliary web (including its very edge), and insert com-
pactly on the extreme periphery of the lens, largely just in front of its
equator.

The Monotreme Retina — The rather thin sensory retina extends
farther forward temporally than nasally in Ornithorhynchus (but not
in Tachyglossus?) , suggesting an importance of the binocular field.

*And the unstriated condition of the sphinaer pupillcc; but there is no reason to think that
this is a new muscle. Iris muscles have been independently evolved several times of course;
but the mammalian sphincter has, in all probability, been inherited directly from the rep-
tiles. Not so the mammalian dilatator.

fMeasured in O'Day's preparations (3.3mm / 1.2mm.); Franz gives 3.0/0.8 = 3.7, but
expresses doubt as to the validity of these figures. Kolmer gives 2.88/. 96 = 3.0 for
Z^dglossus, but his material was preserved many hours post mortem.

670

MAMMALS

There are no blood vessels either in the retinal tissue (as in a few
marsupials and many placentals) or lying on its surface like the hyaloid
or vitreal systems of lower vertebrates. No monotreme has any trace of
a conus papillaris. This complete nutritional dependence of the retina
upon the chorioid is characteristic of light-shunning vertebrates (see pp.
648-58). The disc is small, smooth, and unpigmented in both genera,
circular in Ornithorhynchus and vertically oval in Tachyglossus. Kolmer
describes a peculiar mass of connective tissue which is embedded in the
bulbar portion of the optic nerve in Zaglossus.

Fig. 195 — The visual cells of the lower mammals. xlOOO.

a, single cone, double cone, and rod of Ornithorhynchus. After O'Day.

b, element from pure-rod retina of Tachyglossus. Drawn from a preparation of O'Day.

c, droplet-bearing and droplet-free single cones, double cone, and rod of an opossum, Mar-
mosa mexicana (Australian marsupials have no droplet-free cones and have droplets in both
members of their double cones).

Not only in its avascularity, but in its entire histology, the mono-
treme retina is sauropsidan and might easily be taken for that of a
nocturnal reptile. In Ornithorhynchus, O'Day figures three rows of
outer nuclei, four of inner, and a single row of ganglion cells, and says
that the nerve-fiber layer is thin even near the disc. Tachyglossus, which
is pure-rod, has three layers of outer nuclei (Zaglossus has four) , only
two of inner (Zaglossus has three) , and a decidedly scattered single row
of ganglion cells. Some of the latter are ectopic and lie at various levels
in the inner plexiform layer. The greater extent of summation in the

MONOTREME RETINA; MARSUPIAL EYE 671

echidnas, and the total absence of cones,* implies a stricter nocturnality
than that of the duck-bill; but no great difference in habits seems to
have been noted.

The types of visual cells are direct derivatives of those of the Saur-
opsida (Fig. 195a, b; cf. Figs. 176b, 177a, 193b, pp. 612, 615, 660; and
see Plate I) . In Ornithorhynchus the single and double cones have lost
the paraboloid but have retained the oil-droplet, which was very recently
found to be colorless. The rod and cone nuclei are not differentiated, but
are both 'cone-like' as in all sauropsidans excepting nocturnal birds. In
Tachyglossus the cones themselves have gone. The complete monotreme
visual-cell pattern (of Ornithorhynchus) fits equally well the accepted
idea that the monotremes are a lateral branch of the stock which cul-
minated in the marsupials, and the minority notion that the monotremes
evolved independently from reptiles. The simplification of the cones in
the duck-bill, and their discard in the echidnas, are natural consequences
of adaptation for dim-light activity.

The Marsupial Eye — Marsupials have a nictitating membrane, but it
is never highly developed. Its gland (the Harderian) is present, along
with the lacrimal. A retractor bulbi is present; but no details are on
record concerning the extra-ocular muscles.

The eyeball is perfectly spherical in a very few species and is prac-
tically spherical in all others. The horizontal and vertical diameters are
always equal, and usually exceed the axial length (by up to 10%). This
relationship is reversed in some opossums. The topography of a sagittal
section is always like that in nocturnal and arhythmic placentals (Fig.
196a; cf. Fig. 71, p. 173). The diameter of the cornea is always great
in proportion to the diameter of the eyeball — 66-80% in kangaroos, 82%
and 87% in opossums (Didelphis virginiana and Marmosa mexicana
respectively), 91% in the cuscus {Trichosurus vulpecula). The cornea
is horizontally ovoid only in large kangaroos, in simulation of their
ungulate counterparts.

The sclera is fibrous, entirely devoid of cartilage (except for some
questionable nodules in the marsupial 'golden mole', Notoryctes) . It has
thus taken the final step in the elimination of the cartilage-and-bone
system of the reptilian eyeball wall, and the basically spherical form of
the marsupial eyeball is the expression of this elimination {cf. snakes).

♦Certain in the case of Tachyglossus; probable in Z.<iglossus, but Kolmer's material was too
badly histolized to make possible any study of the visual cells.

672 MAMMALS

Wherever in higher (i e., placental) mammals the eye departs from this
fundamental sphericity and gains the appearance of having a circum-
corneal scleral sulcus, it is owing to the production of a cornea whose
radius of curvature is substantially less than that of the sclera ie. g.,
man).

The cornea has a 4-5-layered epithelium, and no Bowman's mem-
brane; but Descemet's membrane is ordinarily very thick (not, however,
in Marmosa). The cornea is usually uniform in thickness throughout,
but is thinned peripherally in opossums and perhaps in other small-
eyed forms.

The chorioid is usually about as thick as the sclera — hence, thin in
small eyes and thick in large ones. It is heavily pigmented, richly vas-
cular, and ordinarily is built quite as in the placentals. In Didelphis,
however, a choriocapillaris is present only in the pouch young. During
growth to adulthood, pari passu with the maturation of the tapetum
formed from the retinal pigment epithelium and the unusual invasion of
the outer nuclear layer by retinal capillaries, the choriocapillaris is re-
placed by (or becomes) a plexus of plump, thin-walled veins which occupy
the same position against the back of the glass membrane. These alter-
ations bespeak a turning of the visual cells from the chorioid to the
retinal circulation as their source of supplies, owing to the impermeability
of the tapetum. In a very few other marsupials (Dasyurus, Thylacinus,
possibly Sarcophilus and Petaurus) the chorioid is modified by the pres-
ence of a tapetum fibrosum. In Dasyurus viverrinus this nearly fills the
chorioid — squeezing the large vessels and the few thin, pigmented lamel-
lae out against the sclera — and runs practically from ora to ora, though
permitted to reflect light back through the retina only in the superior
half of the eyeground, where the retinal pigment epithelium is devoid of
pigment. It is probably significant that it is only in Dasyurus, Sarco-
philus, Didelphis, and Marmosa (which may once have had a tapetum
like its close relative Didelphis) that any retinal vessels are known to
occur — necessitated, apparently, by the interference of the tapetum with
the nourishment of the retina by the chorioid (see pp. 652-4) . A vestigial
conus papillaris may also occur in marsupials (Perameles, Hypsiprymnus,
and kangaroos generally) . The supply of the retinal capillary bed, where
present, is from paired veins and arteries which radiate over the retina
from the disc. In Dasyurus viverrinus each of these veins (and their
larger branches) is triangular in cross-section and is embedded in the
inner layers of the retina, with its round arterial companion lying on

THE MARSUPIAL EYE

673

top of it in a low glial ridge which projects a trifle into the vitreous.
The iris contains an unstriated sphincter near the pupil margin (as in
other mammals) ; but no marsupial is known to have a dilatator. Both
retinal layers are therefore heavily pigmented. The stroma is likewise
densely pigmented and is richly vascularized, often with many vessels
partially extruded from its anterior surface.

In large eyes the ciliary body forms a broad zone with well-marked
orbicular and coronal regions; but in small eyes, whose lenses are enor-
mous, the ciliary body is reduced about as it is in snakes. In large eyes

Fig. 196 — The marsupial eye.

a, ventral half of left eyeball of a kangaroo, Macropus giganteus. xl. After Soemmerring.

b, inner surface of segment of anterior uvea of a kangaroo, Macropus agilis. After Franz.

c, iris-angle region of cuscus, Trichosurus vulpecula. Redrawn from Franz.

cm- ciliary muscle; cp- ciliary process; cw- ciliary web; i- iris; Ic- limbus corneae; ot- ora
terminalis retina; p- pupil margin.

the ciliary processes are regular, tall, and thin (Fig. 196b) ; and they
are about as numerous as in comparable placentals (e.g., 120 in Tricho-
surus) . Those of small eyes are low, tortuous, and not so readily counted.
A ciliary web can usually be made out. Though no marsupial has yet
been demonstrated to have any accommodation whatever, a small ciliary
muscle is always present. This may present itself as a meridional Briicke's
muscle with exactly the same relationship to the corneal margin as in
reptiles (Fig. 196c, cm). More often, apparently, it contains both
circular and meridional fibers. The circular ones occupy the anterior half

674 MAMMALS

of the muscle in Dasyurus and Marmosa, and in the former genus they
lie toward the scleral side of the muscle. In Didelphis the meridional and
circular fibers are intermingled in small bundles. The anterior tendon in
these three genera, and probably in many others, is formed by a small
mass of unpigmented uveal 'meshwork' tissue which lies against the
anteriormost part of the sclera and extends forward beyond the iris root,
where it tapers to meet the edge of the membrane of Descemet. Between
this tissue and the sclera lies the endothelial canal of Schlemm. These
relationships are essentially those of the human eye. Within the mar-
supial group, then, the ciliary muscle may be situated either as it is in
reptiles, or as it is in placental mammals. The transition seems to be
made simply by the creation of the meshwork 'tendon', dropping the
anterior end of the muscle farther back from the limbus corneas.

The lens is always relatively large; and in the smaller, more strongly
nocturnal types it may nearly fill the globe — as in many small-eyed noc-
turnal placentals, e.g. Mus. The flatter lenses occur, as would be ex-
pected, in the large-eyed arhythmic forms (Fig. 196a; compare Fig.
71 [opossum], p. 173). Even in the flattest lenses there are never more
than traces of the reptilian ringwulst, and the lens is always quite out
of contact with the ciliary processes. The flatness index of the lens may
be little more than 1.0, or as high (in kangaroos) as 1.5. Some sample
values follow:

Horiz. 4> Lens 0 Lens Thick- Index

Species of eye (D) ness (T) (D/T)

Marmosa mexicana

(a mouse opossum) 6.3mm. 4.7mm. 4.5mjTi. L05

Didelphis virginiana

(the common opossum) U.O 7.3 6.0 1.22

Dendrolagus bennetti

(a tree kangaroo) 15.0 8.3 6.7 1.24

Osphranter (robustus ?);

(a rock dwelling kangaroo) 13.0 10.0 1.30

Macropus giganteus

(a ground kangaroo) 27.0 13.0 10.0 1.30

The Marsupial Retina — Through its loss of all of the accessory
structures involved in sauropsidan accommodation (except the ciliary
processes — and these no longer bear upon the lens), the marsupial eye
as a whole is thoroughly mammalian — i.e., placentalian. The retina,

MARSUPIAL RETINA; PLACENTALIAN EYE 675

however, is as reptilian as that of the monotreme. The visual-cell types
are the same ones as in Ornithorhynchus — single and double droplet-
bearing cones, and filamentous rods (which always outnumber the cones
very greatly, in contrast to Ornithorhynchus) . Only minor modifications
of the full monotreme pattern occur in marsupials. Thus in the Amer-
ican opossums some of the single cones lack oil-droplets (see Fig. 195c,
p. 670) ; and in all Australian marsupials so far examined by O'Day,
the double cones have oil-droplets in both their members — a curious
situation which occurs in American marsupials (and in some birds) only
as an occasional anomaly.*

The rod nuclei in marsupials contain only one or two chunks of
chromatin — a differentiation, from the larger and open nuclei of the
cones, which is characteristic of the placentals but not of the mono-
tremes. It is not known whether the rod and cone foot-pieces are also
differentiated in marsupials. The cones of marsupials, like those of all
other mammals, lack paraboloids. This seems a point of some value in
defense of the monophyletic derivation of all the mammals from a single
reptilian stock.

The single and double cones of marsupials and monotremes, from
their oil-droplets (and despite their loss of the paraboloids) , are clearly
the 'same' elements as the corresponding ones of the reptiles. The mono-
treme-marsupial rod is left to be homologized with the droplet-free
element of the sauropsidans (see Plate I). Its increased (nuclear)
differentiation in the marsupials, over that in the monotremes, coupled
with the persistence of the useless oil-droplets in both groups (these are
gone entirely in the placentals!), suggests that the ancestral monotremes
and the original marsupials were diurnal, and that the monotreme-mar-
supial line acquired its rods secondarily through transmutation and
perfected them within the confines of the line (cf. reptiles, birds).

(B) Placentals

The earliest placentals were 'insectivores' of the Deltatheridium type.
In the Mesozoic, these primitive forms diversified and established several
separate lines of ascent. The insectivore type itself persisted (giving off
the still extant Lipotyphla and, later, forms ancestral to the whales) and
culminated in the 'creodonts' — archaic carnivorous forms, of which the

* According to Albarenque, Didelphis marsupialis and 'Azara (= D. azara?) have only
rods. This seems improbable in view of the extremely close relationship of these forms to
D. virginiana.

676 MAMMALS

modern orders Carnivora and Pinnipedia (seals) are fairly direct de-
scendants. From pre-creodonts, there diverged a line which produced
the artiodactyl 'ungulates'* (peccaries, pigs, hippopotami, tylopods
[camels etc.], deer, antelopes, cattle).

The Lipotyphla (hedgehogs, tenrecs, otter-shrews, shrews, moles,
golden moles etc.) comprise the larger of the two groups of living
insectivores. From this stock diverged the smaller branch called the
Menotyphla, the living members of which comprise the tree-shrews and
elephant-shrews. Along the way, the Menotyphla gave off a branch
which bifurcated into the Dermoptera (taguans or 'flying lemurs'' —
Galeopithecus and Galeopterus) and the Chiroptera (bats). The order
Primates also branched off from menotyphlous stock, close to the tree-
shrews ; and the latter, like the higher primates, have secondarily become
diurnal — perhaps the most primitive placentals to have done so.

From a second of the groups of Mesozoic insectivore-like forms, the ro-
dents and lagomorphs arose. In their highest specializations, the rodents
have risen above some other groups whose origins were not as ancient.

A third assemblage of Mesozoic forms gave rise to the modern Xen-
arthra, comprising the sloths, armadillos, and ant-bears. To these Amer-
ican forms the African pangolins or 'scaly ant-eaters', the Nomarthra
may be closely related. The Xenarthra and Nomarthra, if they are thus
related, form a natural order, the Edentata; otherwise the Nomarthra,
deserve ordinal rank. To the 'edentates' in a former, looser sense, the
Tubulidentata (now considered quite unrelated) were once assigned.

The Tubulidentata, represented today only by the aard-varks iOryc-
teropus spp.), the hyracoid-proboscidean-sirenian bouquet, and the peris-
sodactyl ungulates (horses, zebras, tapirs, rhinoceroses) are all deriv-
atives of pro-ungulates which flourished in Cretaceous time and radiated
from still a fourth branch of the Mesozoic radiation of insectivore-
derivatives.

The Eye as a Whole — In so diversified a group of vertebrates — in
contrast to the birds — the eye naturally exhibits a profuse adaptive

*The mammalogical reader will have noticed that throughout this book the old term 'un-
gulate' has been employed. It embraces several orders which are of course widely separated
in modern classification: the Artiodactyla (even-toed) and the Perissodactyla (odd-toed
hoofed forms), the Hyracoidea (hyraxes) and their close relatives the Proboscidea (ele-
phants). (The Sirenia, though never classed as 'ungulates', are connected with the base of
the elephant branch). The nowadays artificial term 'ungulate' has seemed here a conven-
ient word-saver, for the orders embraced by it have eyes which are much alike. From
comparative ophthalmological evidence, no one would be led to believe that the artiodactyl
and perissodactyl lines of descent have actually been separate since almost the inception
of the Placentalia.

THE PLACENTALIAN EYE 677

radiation paralleling that of the group itself. The placental-mammalian
eye has been carried along the ground — rapidly or slowly — and into
trees, into the free air, into the fresh waters, and a mile below the surface
of the ocean. It has been required to work in brightest sunlight and
faintest starlight. It has been asked to inform its owner of an enemy
miles away, and to analyze a tiny object held close before the face. The
placental eye has been able to cope with all of these situations. Only in
complete and permanent lightlessness has it given up, and shrivelled to
a pin-head hidden beneath the skin. This sort of degeneration has oc-
curred several times — in two distinct families of lipotyphlous insecti-
vores, the true, talpid moles {Talpa, Scalopus, etc.) and the golden
moles (Chrysochloris spp.) ; in two families of rodent 'moles', the Spa-
lacidae and the Bathyergidae; and in one additional genus of rodent
(Ellobius) which belongs to the hamster branch of the mouse family.

The adnexa have been discussed on pp. 36-41 (man) and pp. 425-8
(mammals in general) ; and the special features of the sirenians, whales,
and seals have been previously treated (pp. 407-17, 444-8). There re-
mains a great deal which could be said about placentalian eyes, not
much of which can be squeezed into the space allotted here. For detailed
anatomical information the reader will have to turn to such compendia
as that of Franz (1934) , and to the works cited therein.

Functional, harmonious, placentalian eyes range in size from about
a millimeter in the shrews and the smallest bats to that of the great
blue whale, Balcenoptera musculus (145 x 129 x 107mm.). Carnivores,
diurnal primates, and ungulates have the largest eyes relative to body
size. In the lowest orders (Insectivora, Chiroptera, Edentata, Rodentia)
the eye is both relatively and absolutely small, in sympathy with the
nocturnality of these animals and the unimportance of vision in their
lives. Orycteropus however has a large eye (22 x 22mm., 20.5mm. axis) ,
which aligns this form with its ungulate relatives.

The basic shape of the eyeball is the sphere; but a horizontal ellipsoid-
ality, at maximum about as great as it ever is in birds, occurs in some
ungulates and in many large-eyed aquatic forms. The cornea may pro-
trude from the sphere formed by the rest of the globe when it is small
and sharply curved throughout (e.g., man), or its apex may be acutely
curved even though the rest of the cornea blends with the curvature of
the sclera (carnivores) . The axis is somewhat shortened in many ungu-
lates, in which the lens has been moved forward (see Fig. 71, p. 173),
and also in the more fish-like aquatic eyeballs. In Galago and Tarsius,

678 MAMMALS

and to a lesser extent in some other nocturnal prosimians (e.g., Nycti-
cebus), the eye is 'tubular' (Fig. 84, p. 213). In large-eyed mammals,
it is common for the lens and cornea to be shifted nasally as in birds,
and for the ciliary body to be consequently narrower nasally than tem-
porally, chiefly at the expense of the nasal orbiculus, which may be quite
abolished (see cougar. Fig. 71).

The sclera never contains any traces of cartilage. It is usually thickest
in the fundus and thinnest at the equator; but the cornea may be much
thicker than any part of the sclera, or much thinner — the local differ-
ences in the thickness of the fibrous tunic are so various that they cannot
be covered in a few words. A Bowman's membrane is seldom discrimin-
able; but Descemet's layers are always present, and the elastic membrane
may be enormously thick in large eyes. An exceptional cornea is that of
the armadillo (Dasypus novemcinctus), in which the substantia propria
contains many capillaries, even at the apex. These are perhaps required
by the fact that the corneal epithelium, being strongly keratinized, can
derive no sustenance from the tear fluid.

Except where a tapetum lucidum has been produced in it, the chorioid
is usually built as it is in man, but is seldom so thick. It is exceptionally
thin in the squirrel family; but the most unusual chorioid is that of the
large bats (Megachiroptera). In these forms there are 20,000-30,000
conical, vascular papillae which are protrusions of the chorioid, inter-
digitated with the retina and deforming the latter's visual-cell layer (see
Fig. 102a, p. 255). Kolmer found this situation in all sixteen of the
species he studied, but not in any of an equal number of microchiropteran
species. Five structural types of papillae can be recognized; and more
than one type may occur in one species, in different retinal regions.

The iris in large eyes (carnivores and seals, ungulates, whales, pri-
mates) has essentially the same constituents as in man. All of these
mammals have a dilatator, histologically and embryologically resembling
that of man, but with a topographical arrangement which depends upon
the shape of the contracted pupil (see Fig. 85, p. 218). In well-adapted
aquatic placentals (otters, seals, whales), and also in the pigs, the
sphincter occupies the entire width of the iris; and the dilatator may
send fibers into the ciliary body for firmer anchorage. In the smaller,
nocturnally-adapted eyes of all the lower orders of placentals, a dilatator
is ordinarily lacking; but the sphincter is always in evidence and some-
times very large, though always compactly massed near the pupil margin.
Toward the root of the iris, stromal strands may cross the filtration

THE PLACENTALIAN EYE 679

angle and join to the cornea, thus contributing to the 'pectinate ligament'
(or sometimes forming the whole of it) . At the other 'end' of the iris —
the pupil margin — cystic protrusions of the pigmented retinal layers
form the corpora nigra or 'grape-seed bodies' (Fig, 86, p. 219) which
are characteristic of the highest artiodactyls (tylopods, and ruminants
except Tragulus) and also of the highest perissodactyls (horses) . Where
a dilatator is present, the anterior retinal layer is pigmented only slightly
or not at all; otherwise, it is as dark as the posterior layer, as in lower
vertebrates in which it has not partly differentiated into muscle. The
color of the iris is usually dark brown. Where it is not, the color is
generally optical, as in the 'blue' human eye; but lipophores and irido-
cytes may be present in the stroma, as in the cats and some prosimians.

The organization of the ciliary body in all placentals is basically the
same as has been described earlier for man. A corona (bearing true,
vascular, ciliary processes) and an orbiculus (smooth, or bearing only
low meridional ridges) can usually be distinguished. In carnivores how-
ever, the posterior ends of the processes are practically at the ora (Fig.
197, p. 683) ; and in Orycteropus and ungulates, whose corneae are mark-
edly ovoid horizontally, the obligation of the coronal zone to remain
circular (to 'fit' the lens) results in an encroachment upon the iris,
nasally and temporally, by the anterior ends of the processes — so that
these portions of the iris serve as extensions of the base-plate of the
ciliary body, and are rendered immobile as regards changes involved in
the operation of the pupil. In ungulates and in many carnivores the
orbiculus is practically eliminated nasally owing to the existence of
marked nasad asymmetry (see p. 300).

Except in very small eyes, the main part of the ciliary body (apart
from the processes, that is) gradually thickens toward its anterior end,
as in man. This bulk of uveal tissue is not, however, solid muscle as in
the primate eye. Muscle — sometimes considerable of it, as in carnivores
— is almost always present, but is in the form of slender fascicles inter-
spersed with much connective tissue. Anteriorly, the ciliary muscle tends
to have two anchorages: one, by means of the meshwork tissue which
terminates at the margin of Descemet's membrane (as in man — see Fig.
5, p. 10), and another attachment into the anteriormost portion of the
base plate, practically in the root of the iris. Between these two anterior
leaves of the muscle lies a nearly empty space, best visualized by imagin-
ing the human filtration angle to be eroded or extended backward deep
into the ciliary body. This space, 'Fontana's space (s)', is traversed by

680 MAMMALS

delicate strands of uveal tissue which join the base-plate to the sclera.
The anterior limit of Fontana's space — its boundary with the anterior
chamber (with which it is of course actually continuous, between the
strands) — is fixed by the strands or struts which make up the true
pectinate ligament : These are heavy connective-tissue fibers, coated with
mesothelium, which run from the limbal region of the fibrous tunic to
the root of the iris, and support the latter against the tug of the part of
the ciliary muscle attached thereto, and the pull of the sphincter during
the partial closure of the pupil which ordinarily occurs during accom-
modation. The pectinate ligament gets its name from the word 'pecten',
meaning 'a comb', and referring to the fact that its strands are like the
teeth of a comb which has been bent into a circle with the teeth pointing
inward. The strands are best developed in horses, artiodactyls, Orycter-
opus, carnivores, and especially in seals (where there may be not one
'tooth' but several in a given meridian, forming a fan, somewhat like
the situation in reptiles (see Fig. 109, p. 275; Fig. 71, p. 173 [lynx,
cougar, dog, dromedary]; and Fig. 150, p. 446). In the horse at least,
they appear to be continuous with and identical with the material of
Descemet's membrane; and the horse has very similar fibers, with a
circumferential course, massed anteriorly in the meshwork of the iris
angle.

In small, large-lensed eyes with very extensive corneae (in murids and
similar rodents, armadillos, etc.) the whole ciliary body is reduced great-
ly and occupies a relatively narrow zone — sometimes, as in shrews,
forming a simple roll without meridional folds or ridges, quite as in the
snakes. The uveal meshwork tissue, covering the canal of Schlemm and
tapering to meet Descemet's membrane, which so often serves as a
tendon of the ciliary muscle, is still present in these eyes; but the
ciliary muscle is usually wholly lacking. Fontana's space is either tiny,
or else is confluent with the anterior chamber owing to the absence of
a pectinate ligament (as also in some large eyes, e.g. the human). Such
eyes have no accommodation; and for that matter none has ever been
convincingly demonstrated for ungulates — domestic ones, at any rate —
despite the presence of considerable tissue of supposedly contractile
character. In these small eyes, the ciliary processes are so blobby and
irregular that they can scarcely be counted. A very different situation
exists in large placental eyes :

The ciliary processes in large eyes vary in number with the general
size of the eye, as in birds — actually, with the size of the cornea, since

THE PLACENTALIAN EYE 681

it is this which the ciliary body must be thought of as surrounding. They
number about 50-100 in carnivores, 60-100 in seals, 90-130 in ungulates
and whales, and up to 135 in large-eyed rodents and lagomorphs (hares,
beavers). A ciliary web is often present (see Fig. 194b, p. 667); and,
in a vestigial condition, it can be made out in man. The tips of the ciliary
processes touch the lens in a number of mammals, but they are never
fused with it and probably never exert any effective pressure on it in the
few mammals which have useful accommodation (primates, squirrels,
large carnivores). The mechanics of mammalian accommodation are
entirely unlike those of the sauropsidan process, and the difference may
be wholly ascribed to the fact that the primitive mammals allowed a
'circumlental space' to be opened up between the ciliary processes and the
lens, when they threw away the ossicular ring of their reptilian forebears.

Two chief types of processes are distinguished. The more primitive
type is puffy and rugose, like that in monotremes (Fig. 194b, p. 667;
cf. Fig. 6c, p. 14) . This type occurs in all of the lower orders and also
in some of the highest — the artiodactyls and perissodactyls, for example.
A more specialized type, whose differences from the other have no
known functional significance, is the thin, smooth-surfaced, 'knife-blade-
like' process seen in most carnivores and pinnipeds and in some primates
(Fig. 197a). This type has also been evolved by the higher marsupials
(Fig. 196b, p. 673).

The two kinds of ciliary processes are associated with fundamental
differences in the organization of the zonule which are perhaps related
to the extent of accommodation. In forms with thick processes, some of
the zonule fibers arising from the inner surface of the base-plate run for
a space along the floors of the valleys between the processes, and others
run alongside the faces of the processes. As all these fibers curve out
toward the lens, they are quite uniformly distributed both in the aspect
of a sagittal section and in the view of the zonule obtained by removing
the cornea and iris from a gross specimen. The attachments of the fibers
to the periphery of the lens are uniformly distributed both circumferen-
tially and meridionally (Fig. 197d). One cannot speak here of anterior
and posterior 'leaves' of the zonule, for there is no canal of Hannover.

The greatest contrast with this situation is seen in the carnivores, as
exemplified by the domestic cat, studied by Kahmann. Here the ciliary
processes are knife-like, and between every two major ones there is a low
secondary process. Zonule fibers arising from the orbiculus segregate
into paired bundles as they enter the ciliary valleys, and those in each

682 MAMMALS

bundle form a fan plastered against the face of a major process — one
fan against each face. These fibers insert anterior to the lens equator
(Fig. 197c). Other fibers arise from the ciliary epithelium alongside
the roots of the major processes, and pass along their faces and across
the circumlental space to insert posterior to the lens equator. Again
there is no canal of Hannover; but the insertions of the fibers are not
uniformly scattered around the lens, but are grouped at a number of
discrete places — twice the number of the major processes. There is thus
an even more free communication (between the bundles) from the
anterior chamber to the posterior than in the case of ungulates etc.
The anterior surface of the vitreous is plicated where it bulges forward
a bit into each ciliary valley, and its pressure against the posterior zonule
fibers keeps them bowed; but the anterior fibers take straight courses.
The periphery of the lens is scalloped by the discontinuous attachment
of the zonule.

The minor processes also have sheets of zonule fibers against their
flat surfaces. These arise perpendicularly from the anterior part of the
ciliary body and pass to the posterior insertion-zone on the lens. The
insertions are in meridians intermediate between those of the major fans
(Fig. 197b). All zonule fibers thus lie against ciliary-process surfaces.
A frontal section through the ciliary body shows no fiber cross-sections
on the floors of the valleys or in the open spaces of the valleys them-
selves— a great contrast with the ungulates and lower placentals.

According to Kahmann, the primate zonule exhibits still another
fundamental plan: Fibers from the greater part of the orbiculus pass
only to the anterior lens capsule (forming the anterior leaf) , and others
from near the posterior ends of the ciliary processes pass only to the
posterior capsule, forming a posterior leaf. These two masses of fibers
thus cross each other in the coronal zone (the writer is not at all con-
vinced of this). A few of the fibers with orbicular origins insert at the
lens equator, and thus travel across the otherwise 'empty' canal of Han-
nover. Still other fibers, originating far anteriorly, pass to the posterior
capsule and thus compare with the 'perpendicular' fans of the cat; but
in man there are no regular minor ciliary processes for them to cling to.
From these descriptions, it will be seen that where accommodation is
considerable (carnivores; and, to a much greater extent, primates*), the
zonule fibers which will be most relaxed by the contraction of the ciliary

*The zonules of the squirrels should receive as careful a study as Kahmann has given those
of the other strongly-accommodating mammals.

THE PLACENTALIAN EYE

683

muscle are delegated to the anterior surface of the lens, which exhibits
the most elastic deformation. Other fibers, the perpendicular ones, seem
to have been oriented favorably to serve as check ligaments, keeping
minimal the change in curvature of the posterior surface of the lens.

The lens is nowhere so flat as in man and other diurnal primates.
It is perfectly spherical only in seals and in some toothed whales; but it

Fig. 197 — The ciliary region in placental mammals.

a, portion of anterior segment of a carnivore, Felts lybtca. Redrawn, modified, from Franz.
c- cornea; cp- ciliary process; /'- iris; /- limbus corneae; ot- ora terminalis retinje; pi- p>ectin-
ate ligament (three fibers show); s- sclera; sr- sensory retina.

b, diagrammatic thick frontal section in a carnivore (cat), showing paired bundles of zonule
fibers against the faces of the major ciliary processes, and the smaller 'perpendicular' bundles
associated with the minor processes. Based upon a photomicrograph of Kahmann.

c, carnivore (cat); d, ungulate (pig); e, primate (man). Combined from figures of Kah-
mann. Dotted line shows profile of major ciliary process.

<•- cornea; i- iris; /- lens; p- perpendicular fans (see text); s- sclera.

684 MAMMALS

is very nearly so in many murid rodents and in a few other small-eyed,
nocturnal, lower placentals. In carnivores and ungulates it is variously
intermediate in shape; and its relative size is always related to the habits
of the animal with respea to light (Fig. 71, p. 173).

The Retina — The pigment epithelium usually contains relatively little
pigment, which is never migratory (Fig. 20a-c, p. 44). It may contain
reflective material and serve as a tapetum lucidum in itself (opossum,
Megachiroptera) , or in aid of a chorioidal tapetum (dog). Not all
fruit-bats have the reflective substance — it is lacking in most species of
Pteropus, but is abundant in Pteropus h. condorensis, Hypsignathus,
Cynopterus and Epomophorus. It is not apparent whether these differ-
ences relate to differences in the strictness of noctumality of the various
genera.

Usually the placentalian retina is described as being, typically, vascu-
larized. Actually, retinal vessels, with capillary branches passing out
ordinarily as far as the outer plexiform layer, are numerous only in
primates, sciurids, carnivores, and artiodactyls — all, characteristically di-
urnal or arhythmic (see pp. 654-5). In the primitive ruminant Tragulus
(the mouse-deer or chevrotain), there are only superficial vessels, like the
hyaloid or vitreal vessels of ichthyopsidans and snakes. In most perisso-
dactyls there are no vessels, and in the horse they are restricted to a
six-millimeter circle concentric with the disc. There are but few vessels
in lagomorphs, associated there with the horizontal band of medullated
nerve fibers; and there are few or none in the various rodents outside
the Sciuridse. There are no vessels in the Xenarthra, or in the Chiroptera
except for a few superficial capillaries in Pipistrellus pipistrellus. Retinal
vessels thus seem to have arisen several times, independently, in those
placental mammals with the most cones in their retinae; and certain
embryological differences appear to bear out this conclusion. In murids,
for example, the few adult retinal vessels are formed directly by the
embryonic vasa hyaloidea propria, whereas in primates these atrophy,
and the definitive vessels bud out from the central retinal artery and
vein in the optic-nerve head.

The lamination and the laminal purity of the placentalian retina are
only ordinary, and quite well exemplified by the human retina (Fig. 19,
p. 43 ) . Only in the diurnal squirrels and particularly in the prairie-dogs
(Cynomys spp.), and there only in the dorsal region, does the mam-
malian retina approach that of the birds in the segregation of inner-

THE PLACENTALIAN RETINA 685

nuclear elements and in the stratification of the inner plexiform layer
(c/. Fig. 193a, p. 660).

Most placentalian groups have duplex (rod-and-cone) retinae, but in
the lowest orders it seems to be the rule for only rods to be present. The
cones are the simplest imaginable — all single, without paraboloids, oil-
droplets, or myoid extensibility. There are no cones in the armadillo,
possibly none in any edentate. All of the bats have only rods. Among
the Lipotyphla, the hedgehogs are pure-rod according to most inves-
tigators, though Menner found a few cone-type nuclei. The tree-shrews
(Tupaia et al) should have many cones; but the shrews have few or
none.* There are probably many more pure-rod rodents besides the
guinea-pig, and no cones have been reported by modern investigators
for any prosimian below the true lemurs"*", or by any of the half-dozen
investigators who have studied various species of Aotus.

The rodents characteristically have great numbers of excessively slen-
der rods, like those of the rodent-like opossums (see Fig. 23f and g,
p. 55). Slender rods are also the rule in nocturnal primates and carni-
vores, and in the fruit-bats. In all such forms the outer nuclear layer is
naturally very thick, with up to 16-17 rows of nuclei. The inner nuclear
layer ini placentals rarely contains more than four or five rows, except
in Tupaia and in diurnal squirrels, where it may be several times as thick
as the outer (c/. Fig. 72, p. 177). The ganglion cells usually form but
one layer (in which they are often widely separated), except in an area
centralis (where any) and in the neighborhood of the primate fovea.

The more slender and numerous the rods, and the fewer the cones,
the more likely it is that the rod and cone nuclei will be found markedly
differentiated from each other in size, shape, and chromatin distribution
(see p. 57).

The cones of most of the placentals which have many of them are
much like those of man as a rule (Figs. 19, 22f; pp. 43, 54). In flying-
squirrels and ungulates, however, their 'myoid' regions are more or less
elongated; and in diurnal squirrels (except prairie-dogs) there appear to
be two types of single cones, one bulky proximally and slender distally,
the other slender proximally and plumper distally. In prairie-dogs how-
ever the cones are all alike, very slender, and not thus pseudostratified.

*MIle. Verrier found all the cells alike (and, from her drawings, rods) in Crocidura
mimula; but in C leucodon and C. aranea there are more cones than in mice, according
to Schwarz.

tKolmer claims a few for Nycticebus tardigradus, but Detwiler found none in this loris.

686 MAMMALS

Pure-cone retinae are unknown in mammals outside of the Sciuridae —
none occur even in primates, though some of these (e.g. Callithrix
jacchus, Cercocebus torquatus) do have many more cones than man.
Favorable material of Tupaia has never been studied; and there are still
other mammals outside the squirrel and monkey tribes which are re-
putedly strongly diurnal, and whose retinae would bear investigation:
Ochotona, Dolichotis, Procavia, Cynictis, Suricatd, et al.

The Early History of the Placentalian Eye — The simplicity of the
placentalian visual-cell pattern is striking, when one considers that in
the lower mammals each of the standard reptilian-avian cell types is
easily recognizable. No placental is known to have double cones, or
oil-droplets in its single ones.* Obviously the whole sub-class must have
been pulled through some sort of ancestral knot-hole : the 'original'
placental mammal must have 'had a way of life which brought about
these peculiarities and doomed all of its descendants to exhibit them.

The whole organization of the monotreme eye is, as we have seen,
reptilian. If we think of it as a reptilian eye, its oddities seem logical
consequences of a strong nocturnality of long standing. The reversion
of the intra-ocular muscles from a striated to an unstriated condition
shows that in the first mammals accommodation became unimportant,
and it was never necessary for them to close the pupil quickly — presum-
ably, because they never exposed themselves to bright light. Accommo-
dation is of no value to a strongly nocturnal eye — especially one which,
though perhaps relatively large for the animal, is small in absolute
dimensions. The discard of the scleral ossicles and the practical discard
of the ringwulst of the lens allowed the monotreme eye to become
rotund, took the ciliary body out of contact with the lens, and made
forever impossible any return to the sauropsidan method of accommo-
dation. Though the persistence of the retinal oil-droplets suggests that
the early monotremes may have been sufficiently diurnal to have retained
the reptilian eye quite unchanged, the nocturnality which eventually
supervened accounts for the condition of the modern monotreme organ.

The marsupial eye, though secondarily arhythmic in capacity in its
highest expression (in ground kangaroos) , bears the very same stigmata

*Little shrinkage spaces at the distal ends of the cone inner segments have been all too
often mistaken for oil-droplets — even by such careful workers as Kolmer. Examination of
the retina in its fresh condition, and after fixation with osmic acid, will always demonstrate
the presence or absence of real oil-droplets.

EARLY HISTORY OF THE PLACENTALIAN EYE 687

of a former universal nocturnality — perhaps even more complete than
that of any monotremes, Hving or dead, since even the scleral cartilage
has not been kept. In the opossums, which are the most archaic of living
marsupials and hence, so to say, have had the most time in which to
get rid of useless structures, some of the single cones have lost their
oil-droplets.

The placental mammals must have gone farther in adaptation for
dim-light activity, early in their history, than the marsupials have ever
done. Their eyes are in fact best understood not by comparison with
those of the lower mammals, but by comparison with those of the snakes.
The early snakes so completely lost the reptilian assortment of special
ocular structures that when the snake eye was rebuilt, upon the return
of the snakes to the earth's surface, it ended up as a spherical organ with
an entirely fibrous wall, with the lens and ciliary body out of contact
(necessitating a new and special method of accommodation), with a
wholly new set of visual cells, and (eventually) a yellow lens as a sub-
stitute for the ancestral diumal-lacertilian yellow oil-droplets. To a
degree, the placentalian eye incorporates equivalent changes and sub-
stitutions. The 'original' placentalian eye was of course not really degen-
erate like that of a mole or mole-rat, but it did take several steps down
the same path which the eye of the incipient snake followed to its
bitter end.

Whether the placentals evolved directly from nocturnal marsupials,
or turned nocturnal after a derivation from diurnal common ancestors
of the modern marsupials and the placentals, we cannot know; nor
would the knowledge have much importance. We can be sure that at
an early period in placentalian evolution, the only placentals on earth
were so thoroughly nocturnal that their eyes had no stiffening structures
to keep them from being spherical, had large pupils and large, simple
lenses with no trace of a ringwulst and no contact with the ciliary body,
had rudimented intra-ocular muscles which were unstriated and did not
include a dilatator pupillae, and had no accommodation whatever.

Now, what was the retina like in these strictly nocturnal, 'bottle-neck'
insectivores? Apparently all of the lowest living orders of placental
mammals have pure-rod retinae. But the higher ones have both rods and
cones. Do the cones of the higher placentals represent sauropsidan-
monotreme-marsupial cones which squeezed through the primitive in-
sectivoran knot-hole, or are they somehow new?

688 MAMMALS

Placentalian cones are all alike in certain respects: they are all only
single, without paraboloids, and without oil-droplets. These similarities
are negative, and really mean that placental cones are cones reduced to
their lowest structural terms. Naturally they would be alike, even if
those of the tree-shrews, the higher primates, the duplex descendants
of the pre-creodonts (i.e. carnivores, artiodactyls) , and the duplex de-
scendants of the Cretaceous pro-ungulates (/. e. hyracoids, proboscideans,
perissodactyls) all represent independent productions of new cones in
erstwhile pure-rod retinae.

The absence of the paraboloid in placentals is no proof of an identity
of placental cones with those of monotremes and marsupials. The latter
groups have lost the paraboloid, to be sure; but the cones of placentals
would not be expected to have evolved them even if those cones are
'new'. Paraboloids occur only in the cones of groups which have retinal
photomechanical changes, and the paraboloid has been claimed to be a
reserve of food which furnishes the energy for the activity of the cone
myoid. The cones of lampreys and elasmobranchs naturally have never
produced them, nor have the cones of snakes, which are certainly 'new'
cones.

If the placentalian cone represents the reptilian droplet-bearing single
cone, then one can understand its lack of the oil-droplet icf. opossums) ;
but what has become of the reptilian double cone, so stubbornly per-
sisting in even the most strongly nocturnal of the lower mammals except
where all cones have been lost (Tachyglossus)? Elsewhere above the
fishes,* double cones have never been either discarded, or transmuted
into rods, without the matching single cones also undergoing discard
or transmutation.

It seems highly significant that the placentalian cone has no con-
sequential capacity for color vision except in the primates, where color
vision has evolved within the group (see pp. 518-21). If the duplex
placental mammals had had continuously duplex retinae ever since the
placentals originated, then all such mammals, and not the simians alone,
should have as complete a color-vision system as that which character-
izes the Sauropsida; for, they should have retained that same system —
having retained the same cones.

All in all, it seems most probable that at one time the only living
placentals had no cones, but only the rods which we see in the lower

*The chondrosteans and Neoceratodus have apparently lost ancestral double cones
Plate I.

EARLY HISTORY OF THE PLACENTALIAN EYE 689

mammals, and that subsequent placentals evolved duplex retinae from
pure-rod ones just as the Boidae or their immediate ancestors had to do
(see Plate I). The eye of man, with its pretty-good accommodation, its
fovea, its miscellaneous yellow filters, and its capacity for color vision,
possesses in substantial degree the physiological capacities of the stand-
ard sauropsidan eye as we see it in the lizard or the bird. But it has
gained these powers through a lengthy process of re-differentiation, which
was carried out largely within the confines of the primate order itself.

Plate I (opposite) — Tentative schema of the evolution of the visual cells in vertebrates.
(Pertains to the discussions of the retina in Part III).

KEY

TO S Y

M B 0 L S--

A

single cone

D single rod

lA 'intermediofe' element

Aa

double cone

Dll double rod

Q de-differentioted cell

AA

twin cone

^ 'green' rod

i rhodopsin present

. oil-droplet (pigmented) •

disappearance of type

o oil-droplet (colorless)

alternative derivation

CORRIGENDA AND ADDENDA

P. 59, figure legend, add: x- paranuclear body.

P. 72, I. 24, for: pure-cone read: nearly pure-cone.

P. 99, 112: Dunlap and Loken (1942) have reported 'cures' of Daltonism.

P. 106, figure legend, I. 9, for: and read: and.

P. 109, I. 5, for: amphibians read: fishes and amphibians.

P. 150: Cajcilians have no pigment migration.

P. 184, II. 32-33: See entry below for p. 568

P. 187: Some owls have deep foveas.

P. 195, II. 7-i, for: except in birds read: except in non-strigine birds.

P. 200, for: Petromyzontidae read: Petromyzonidae.

P. 201, for: Ochotona, Castor read: Ochotona, Castor, Dolkhotus.

P. 203, 1.8, for: Anniella read: Aniella; II. 35-37: c/. p. 671.

P. 221, for: Dryophis & Thelotornis read: Dry o phis, Dryophiops and

for: Rhynchops read: Rynchops; [ Thelotornis;

for: Indris read: Indri. (Same change, p. 228, I. 14).

P. 223, Fig. 87 legend, for: Hyperlius read: Hyperolius;
for: quoyi read: gayi.

P. 236, I. 17, add: Alburnus bipunctatus, Bliccopsis abramo-rutilus (Blicca
bjorknax Rutilus rutilus hybrid).

P. 237, I. 16, for: Evermannella read: Evermanella.

P. 240: Note p. 585, last H.

P. 254, 1.33, and p. 270, I. 6, for: Macrochiroptera read: Megachiroptera.

P. 266, figure legend, II. 6-7, for: only the ventral one read: none.

P. 270, figure legend, for: punctatus read: punctatiim.

P. 273: Urodeles have no pupillary nodules.

P. 312, 1.9, for: Elliott read: Elliot.

P. 386, 1.8, for: Galeorhinidce read: Galeorhinidas;
1. 14, for: Raja read: Raja.

P. 409, figure legend, for: Pettit read: Petit.

P. 434, figure legend, for: Schneider and von Orelli read: Schneider-von Orelli.

P. 450: Delete Aniella (see footnote, p. 625). Under 'significance', for: fos-
sorial read: fossorial or nocturnal. Under 'lids fused' and
opposite 'vestige', add: Lizards: diurnal geckoes.

P. 452, I. 25, for: retractor bulbi muscle read: rectus muscles.

P. 494, I. 18, for: colorvision read: color vision.

P. 506, I. 2, for: Orbelli read: Orbeli.

P. 511, 1.26, for: Abbot read: Abbott.

P. 518, 11. 33-34: See entry below for p. 568.

P. 527, II. 8, 9, 14, and p. 535, I. 18, for: Babak read: Babak.

P. 556, I. 22, for: homologous read: homoiologous.

P. 561, figure legend, for: in Myliobatus aquila read: in Lamna cornubica
and Myliobatis aquila. (See next entry).

P. 568, last H: Rochon-Duvigneaud (1939) figures distinct cones (and rods)
for Lamna cornubica.

P. 589, re Cladistians: According to Rochon-Duvigneaud (1939), Polypterus
congicus has only rods, the inner segments of which are plump
and cone-like (i.e., as in dipnoans? with oil-dropIets?); and the
horizontal-cell processes are thin icf. pp. 591, 598).

P. 608, sub-index: Delete entry for p. 72.

P. 663, col. 2, 1.9, for: reraction read: refraction.

P. 676, I. 10, delete: taguans or;

1. 22: comma at end of line belongs at end of I. 20.

P. 686, I. 2, for: Callithrix read: Hapale.

692

BIBLIOGRAPHY

NOTE: The list of titles which follows is but a tiny portion of the whole
literature of the eye. Its items have therefore been selected carefully. I have
tried to include the sources of borrowed illustrations, and the more important
works of all authors specifically mentioned in the text — in some instances citing
only the author's later contributions, the bibliographies of which will provide
leads to the earlier work of that author and others. I have included a number
of books, compilations, and monographs whose long lists of literature will give
the beginner a good start in compiling his own card-catalogue of those phases
of the subject which interest him most. Certain of these major works (some of
them now obsolete, but definitive in their time) should perhaps be the first to
be consulted by the new investigator of the vertebrate eye, and these have been
starred (*). The more important of my own papers are also listed, and I have
ventured to star a couple of those whose bibliographies contain a number of
important references which have been omitted here.

I have included a few non-ophthalmological items (and where their titles are
not self-explanatory, I have annotated them) ; but I have made no attempt to
list all of the sources of my zoological and ecological information, for to cite
any reasonable number of pertinent works would serve only to give them undue
emphasis. Some zoological writings are mines of information; but many a book
must be read through for the sake of gaining a single ophthalmological fact.
The beginning investigator of the vertebrate eye must read omnivorously in the
natural-history field, and is well advised to maintain a correspondence with the
curators of the nearest research museum of vertebrate natural history.

The reader will note that the non-clinical literature of the eye is sadly scat-
tered— there have been only two periodicals, both short-lived, which were en-
tirely devoted to comparative ophthalmology. These were the Z.eitschrijt fiir
vergleichende Augenheilkunde (7 vols., 1882-93) and the Archiv fiir vergleich-
ende Ophthalmologic (4 vols., 1910-14). Each of these contains many valuable
abstracts as well as original contributions. The student should also make the
acquaintance of the Journal of the Optical Society of America, the extinct
American Journal of Physiological Optics (7 vols., 1920-6), and the Unter-
suchungen aus dem Physiologischen Institut des Universit'dt Heidelberg (4
vols., 1877-82). Aside from the latter, which contains practically all of Kiihne's
work on rhodopsin, the only general journals which have been heavily com-
parative-ophthalmological are the Jenaische ^eitschrift fiir Naturwissenschafi
and the Z.eitschrift fiir vergleichende Physiologic. The student simply must
keep constant watch for new contributions in all of the morphological, physiol-
ogical, and ophthalmological journals.

Following the list of titles is a list of names, preceded by a separate explan-
atory note, which is intended to help the student to locate current literature.

693

694 BIBLIOGRAPHY

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1930. Versuche iiber den Farbensinn der Lemuren. Zeits f. vergl. Physiol., Bd. 12, pp.
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1939. Das Auge des Argyropelecus hemigymnus. Morphologie, Bau, Entwicklung und
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1939. The flicker response contour for the gecko (rod retina). Jour. Gen. Physiol., vol.
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1941. The simplex flicker threshold contour for the zebra finch. Jour. Gen. Physiol.,
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1938. The life story of the fish. New York and London: D. Appleton-Century Co., Inc.
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Fritsch, G.

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1914. Der Farbenwechsel und die chromatische Hautfunktion der Ticrc. In: Handbuch
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1935. Ober die Existenz des Canalis hyaloideus bei Mensch und Tier. Arch. f. Ophthal-
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1935. Two types of retina and their electrical responses to intermittent stimuli in light
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1936. Die Elektrophysiologie der Netzhaut und des Sehnerven mit besonderer Beriick-
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1939. Principles and technique of the elearophysiological analysis of colour reception with
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1938. Selective effects of different adapting wave-lengths on the dark adapted frog's
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1937. The electrical responses of light-adapted frogs' eyes to monochromatic stimuli.
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1935. The eye of the monotreme. Echidna hystrix. Jour. Morph., vol. 58, pp. 279-284.
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1939. Vascular obliteration for various types of keratitis, its significance regarding nutri-
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1933. Trichromatic vision in the pigeon as illustrated by the spertral discrimination
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SCHIEFFERDECKER, P.

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BIBLIOGRAPHY 715

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718

BIBLIOGRAPHY

NOTE: The list of names which follows is offered the beginning investigator
as a check-list of workers, most of them still living and active, who have been
particularly productive in the field of this book in recent years or are likely to
be especially productive in the future. These are names to watch for in perusing
past and future issues of the bibliographic periodicals. Not all of these investi-
gators are wholly 'trustworthy' — two or three are decidedly not, but are included
here because they are too prolific to be ignored.

In the accumulation of titles and abstraas of the current non-clinical litera-
ture and that of recent past years, the student will find the following publi-
cations helpful: American Journal of Ophthalmology (abstracts); Anatomischer
Anzeiger (international bibliography); Archives of Ophthalmology (abstracts);
Biological Abstracts; British Journal of Ophthalmology (abstracts, transac-
tions); Chemical Abstracts; Physiological Abstracts (and the Annual Review of
Physiology); Psychological Abstracts; Quarterly Cumulative Index Medicus
(titles with subject classification); Scientiae Naturalis Bibliographia (titles);
Special Reports of the Committee upon the Physiology of Vision, {British)
Medical Research Council (each an extensive research or review, with a com-
prehensive bibliography); Z.entralblatt fiir die gesamte Ophthalmologic und
ihre Grenzgebiete (abstracts) ; and Zoological Record (titles with subject clas-
sification) .

Adelmann, Howard B.
Allen, Frank
Arey, Leslie B.
Atsatt, Sarah R.
Bartley, S. Howard
Bierens de Haan, J. A.
Birukow, Georg
Bishop, George H.
von Bonin, Gerhardt
Brecher, G. A.
Breder, Charles M., Jr.
von Buddenbrock, W.
Bull, H. O.
Butcher, Earl O.
Chard, Ray D.
Chase, Aurin M.
Clark, W. E. LeGros
Cobb, Percy W.
Cogan, David G.
Crozier, William J.
Curtis, Brian

Detwiler, Samuel R.
Franz, Viktor
Fry, Glenn A.
Gliicksmann, A.
Graham, Clarence H.
Granit, Ragnar
Gresser, Edward B.
Grether, Walter F.
Gundlach, Ralph H.
Halstead,WardC.
Hamilton, W. F.
Hartline, Haldan K.
Hecht, Selig
Holmberg, T.
Honjo, Ichijiro
Hosoya, Y.
Kahmann, Hermann
Keeler, Clyde E.
Kliiver, Heinrich
Kolmer, Walther
Krause, Arlington C.

BIBLIOGRAPHY

719

Kravkov, S. V.
Lashley, Karl S.
Lasker, Gerhard
Leinfelder, P. J.
Ludvigh, Eiek
Lythgoe, Richard J.
Mandelbaum, Joseph
Mann, Ida C.
Marshall, Wade H.
Matthews, Samuel A.
Meader, Ralph G.
Menner, Erich
Merker, E.
Moore, George A.
Munsterhjelm, A.
Murr, Erich
O'Leary, James L.
O'Day, Kevin J.
Osbom, Clinton M.
Pitt, F. H. G.
Polyak, Stephen
Roaf, H. E.

Rochon-Duvigneaud, Andre
Riggs, Lorrin A.
Sachs, Erich
Scharrer, E.

Schmidt, W. J.
Skolnick, Alec
Smith, G. Elliot
Stroer, W. F. H.
von Studnitz, Gotthilft
Sumner, Francis B.
Sverdlick, Jose
von Szily, A.
Talbot, Samuel A.
Tansley, Katharine
Therman, P. O.
TretjakoflF, D. K.
Vernon, M. D.
Verrier, Marie Louise
Wald, George
Welsh, John H, Jr.
Wilson, F. H.
Wissler, H.
Wolf, E.
Wrede, C. M.
Wright, W. D.
Wunder, W.
Young, J. Z.
Zerrahn-Wolf, G.
Zewi, M.

ABBREVIATIONS AND SYMBOLS

,A.u.

=

Angstrom unit = 0.1 m/i

ca.

=

circa = approximately

cf.

=

confer - compare

e-g-

=

exempli gratia = for example

et al

=

et alii = and others

i.e.

=

id est = that is

\

=

lambda = symbol for wavelength

m.

=

meter = 3^.38 inches

At

=

mu = micron = .001 mm.

mm.

=

millimeter = .001 m.

mil

-

millimicron = .001 /i

TT

-

pi = 3.1416

</>

=

phi = symbol for diameter

q.y.

=

quod vide = which see

sp.

=

species

spp.

=

species (plural)

s.s.

=

sensu strictu - in the strict sense

vs

-

versus — as against

v.i.

-

vide infra = see below

Y.S.

-

vide supra - see above

>

=

greater than

<

=

less than

V

-

square root of

-

to (ratio sign)

720

INDEX AND GLOSSARY

NOTE: Page numbers in boldface indicate illustrations (and may also refer to textual
matter pertaining to the item). A starred (*) page number indicates that the item will be
found defined or characterized on that page. Other terms (not clearly defined in the text,
or likely to be unfamiliar to the reader) will be found defined or charaaerized here as re-
gards the senses in which they have been used in the text. The arrangement of sub-items is
alphabetical except in certain instances where a taxonomic arrangement seemed likely to
prove more convenient.

birds, 440-442, 441, 647
mammals, 442-448
seals, 445-448
camera analogy for, 7
chief methods of, 251, 257-258, 438, 686

evolutionary change, 417
convergence and, 314, 318, 328, 330
devices which obviate, 253-257, 255
eyeshine and, 231
feeding habits and, 286
locomotor speed and, 253
mechanisms, distribution of, 272-273
(Table VIII), 417, 681, 686,
692 (entries for pp. 266, 273 )
'negative' and 'positive', 251, 597
-reflex of pupil, 156
role of pupil in, 272-273 (Table VIII),

692 (entries for pp. 266, 273 )
visual acuity and, 283-284
visual field and, 299-300
why needed, 26, 30-32, 249-253, 588, 686
taxonomically:
lampreys, 258-260, 265, 268
elasmobranchs, 251, 259-260, 265-267,

272-273, 381, 429
teleosts, 161, 260-261, 265, 299, 401-402,
other fishes, 263-264 [583-584,586

amphibians, 265-268, 266, 429, 436, 597
sauropsida, 269-283, 275, 280, 295, 299,
456, 647-648, 681, 686
lizards, 623-624, 632
snakes, 456, 630-631, 633
birds, 647-648, 651, 655-656
mammals, 283-288, 409-410, 414, 669,
673, 680-683
man, 27, 30-36, 31, 35, 194, 440, 681-
683
Acerina (teleost), retinal tapetum lucidum
acetylcholine, 529* [in, 236

acid

effea of

on photomechanical changes, 151
on tapetum lucidum elements, 235
retinal adaptation and, 151

aard-vark: Orycteropus, q.v.
AbastOT (reptile: a rainbow snake)

accommodation in, 438

chorioid of, 629

pupil of, 225

scleral pigment in, 628

spectacle of, 450

visual cells of, 154, 640
Abbott, 511, 692 (entry for p. 511)
Abelsdorff, 500-501, 646, 651, 657
abiotic light, 375*

protection from, 375, 417
Ablepharus (reptile: a lizard), spectacle of,
Abramis (teleost: bream) [450

retinal tapetum lucidum of, 236-237

rhodopsin visible in living, 231
Abramowitz, 534
abyssal fishes (see deep>-sea fishes)
Acanthophis (reptile: death adder)

sclera of, 627-628

slit pupil of, 221, 225
dilatator of, 630
Acanthopterygii : spiny-rayed teleosts;

adipose lids in, 383 [391*, 576*

charaaeristics of, 391-392, 576

double (?) cones in, 586-587

guanin tapetum lucidum in, 236

horizontal cells of, 585

ocular characters of, 576-578

spectacles in, 460-461
Accipiter (bird: a hawk)

muscle of Miiller in, 646
accipitrines : hawk sub-family

visual trident of, 307-309
accommodation

air-and-warer vision and

the essential problem in, 430

taxonomically:

teleosts, 430-433

amphibians, 436

chelonians, 436-437, 609-610, 614, 622

crocodilians, 436, 614

snakes, 282-283, 438, 456, 630

722

INDEX AND GLOSSARY

acid — cont'd
uric

and guanin, 235
in photophores, 235
Acipenser (chondrostean: sturgeon), 570
accommodation in, 264
argentea of, 570-572
chorioid of, 570-571
conjunctival bones in, 569
cornea of, 569-570
habits of, 150, 200, 381
iris of, 571-572
lens of, 160, 570-571

-muscle papilla (?) in, 571-572
suspensory ligament of, 571
ocular shape in, 381, 570
orbit of, 569
pupil of, 150, 160, 220
retina of, 242, 572

photomechanical changes in, 150
pigment epithelium of, 238-239, 242
sclera in, 415, 569-570
tapetum lucidum of, 238-240, 242, 570-
taxonomic position of, 136 [571

visual cells of, 54, 242, 570, 572-573, 688
oil-droplets of, 200, 202, 242
AcTOchordus (reptile: elephant-trunk snake)

dorsal binocular field of, 293, 438
adaptation, visual (see vision, photopic and

scotopic)
adder, common: Vipera, q.v.
adipose lids (see lids, adipose)
adnexa: lids -f muscles -i- glands (see also
nictitating membrane, speaacle)
taxonomically:
lampreys, 556-557

elasmobranchs, 428-429, 432, 563-565
chondrosteans, 569
holosteans, 573-574

teleosts, 381-384, 386-387, 431-432, 578
lungfishes, 589
amphibians, 407, 418-419, 421, 436, 592-

594, 601, 604-606
chelonians, 421-423, 437
crocodilians, 421-422
Sphenodon, 420-421, 617
lizards, 421, 423
birds, 420-421, 424-425, 440-441, 642,

644
mammals, 408, 412-414, 425-427, 443-
445, 665-666, 671
man, 36-41, 37, 39
adrenalin, 151, 478, 529, 535-536, 540, 543
aestivation: summer period of dormancy;

223, 263
afferent: said of nerve-fibers or impulses
which conduct or travel toward
the central nervous system

arter-image

complementary, 93*, 471
in hemianopia, 336

positive, 350*
Agamida (reptiles: a lizard family)

continuity of lids in, 423

dermal color changes in, 538

eye movements in, 306

former placement of Sphenodon in, 616
Agkistrodon (reptiles: moccasin snakes)

habits, pupil, retina of, 165

visual cells of, 166, 639-640
aglossal: tongueless (from Aglossa, a

division of anurans)
Agonus (teleost), fovea in, 304
Ahcetulla (reptile: a colubrid snake), pupil

of, 221, 225
air, vision through (see terrestrial activity)
Albarenque, 675
albatross: Diomedea, q.v.
albedo, 493, 530*

responses to, 530-536, 545
albinos

lentiflavin in, 199

ostracism of, 466
Albula (teleost: ladyfish), leptocephalus in,

406
Alburnus (teleost: a cyprinid), retinal tape-
tum lucidum in, 692 (entry for
p. 236)
Alcedo (bird: a kingfisher), 'bifocal' lens

of, 257, 442
Alligator (reptile: a crocodilian)

accommodation and refraction of, 272-
273, 279

adnexa of, 42 I -422

area centralis of, 187

conus papillaris in, 615, 653

dermal color changes in, 542-543

elevation of eyes in, 443

eyeshine of, 240

lens of, 620

ocular structure in, 613-616, 654

pupil of, 220

Purkinje shift in, 496

retina of, 615-616

tapetum lucidum of, 240, 615-616, 654

visual acuity of, 207

visual cells of, 615-616

visual fields of, 294
Alosa (teleost: shad), visual cells of, 586
altricial : said of birds hatched featherless

and helpless; 644
Alytes (amphibian: obstetrical toad)

scleral cartilage of, 595

vertical pupil of, 223
Ambloplites (teleost: rock 'bass'), eye color
change in electric shock in, 551

INDEX AND GLOSSARY

723

Amblycephalidas (reptiles: chunk-head snake

habits of, 201 [family)

pupils of, 221
Amblyopsidje (teleosts: a cave-fish family)

eyes of, 387-388

spectacle in, 450
Amblyrhynchus (reptile: marine lizard),

eye and habits of, 438
Ambystoma (amphibian: a salamander)

compared with lungfish, 604

dermal color changes of, 527, 537

ependymal cells of, 573

lack of ciliary muscle in, 602

visual cells of, 599
summation, 603
AmbystomidcB (amphibians: a urodele

sclera in, 601 [family)

taxonomic position of, 600
AmeiuTus (teleost: bullhead catfish)

branched optic nerve of, 367

retina of, 147, 176,585

visual cells of, 176
migrations of, 147
Amid (holostean: bowfin)

annular ligament of, 574-575

argentea of, 570

chorioid of, 574

habits of, 150, 200, 381, 518

iris of, 574-575

lens, 575

-muscle papilla of, 264, 273, 575

ocular shape in, 381, 574

oculorotatory muscles of, 573-574

optic nerve and disc of, 576

possible color vision of, 518

pupillary changes in, 150

retina of, 518, 576

photomechanical changes of, 150

sclera of, 574

taxonomic position of, 137

visual cells of, 59, 200, 586-588, 587, 591,

vitreal vessels of, 575, 589, 605 [600

yellow cornea of, 200, 202, 591
amniotes: reptiles -i- birds -i- mammals; 588
Amphibia, 368*; (Anura, Ccecilia, Stego-
cephali, Urodela, qq.v.); sub-
index, p. 592, and pp. 592-606
amphibious activity, eye and vision in, 368-
369, 429-448; see also aquatic

adnexa and, 429-430 [artivity

TAXONOMICALLY:

teleosts, 431-436, 453
amphibians, 436
chelonians, 436-438
crocodilians, 436
lizards, 438
snakes, 438
birds, 425, 439-442

mammals, 442-448
Amphiodon (teleost: a clupeoid), adipose
Amphioxus: a chordate, q.v. [lids of, 383

anterior pigment spot of, 120

ependymal cells of, 120, 128

Hesse's organs of, 124-126, 128

infundibular organ of, 120, 128

Joseph's cells of, 120, 126, 128
Amphisbajnidse (reptiles: a fossorial lizard

cranium in, 634 [family)

eyes of, 625

spectacles of, 450, 458
Amphiuma (amphibian: a salamander),

eye and habits of, 407
Amphiumidse, 600* •

Amyda (reptile: soft-shelled turtle), fovea

of, 186-187, 190, 305, 611-612
Anabas (teleost: climbing perch)

annular ligament of, 580

habits of, 431

refraction and accommodation in, 272-

spectacle of, 450 [273,431

Anableps (teleost: four-eyed fish; see frontis-
piece)

comparison with other 'bifocal' eyes, 257,
439-440, 442

eye and habits of, 434-436, frontispiece
Anacanthini, 391*, 576-577*
anadromous: said of fishes which live in the
sea but breed in fresh water; 371-
372, 375, 569
anatine ducks, ciliary muscles of, 441
Anchoviella (teleost: an anchovy), spec-
tacle of, 460
anchovies (teleosts, near herrings)

guanin in retinee of, 585

spectacles of, 450, 454, 460-461
Ancydopsetta (teleost: a flounder), dermal

color changes of, 482
Anelytropidae (reptiles: a fossorial lizard

eyes of, 625 [family)

spectacles of, 450
anglers: Lophius, q.v.
Anguidae (reptiles: a lizard family; see

Anguis, Ophisaurus)
Anguilla (teleost: common eel)

contractile pupil of, 220, 222

eye and life-cycle of, 406

spectacle of, 454
Anguis (a legless anguid)

eyes of, 633

visual fields of, 294
Aniella (reptile: a worm-lizard, q.v.; and
see p. 692, entry for p. 203)

ocular structure in, 625

oil-droplets of, 203, 627

spectacle in, 450 (error; see p. 692, entry
for p. 450), 625

724

INDEX AND GLOSSARY

animated cartoons (see motion pirtures)
aniage: earliest recognizable developmental
anoles: Anolis, q.v. [stage of a structure

Anolis (reptile: an iguanid lizard)
dermal color changes of, 540-542
lid movements in, 423
Anomalops (teleost), photophore beneath

eye in, 396-397, 405
Anomaluridae, 664*

Anoptichthys (a caverni colons teleost), vari-
ability of eye in, 210, 387-388
anoxia: deprivation of oxygen
ant-bears: placentalian ant-eaters, except

aard-varks and pangolins
ant-eaters (mammals)

banded: Myrmecobius (a marsupial)
placentalian (^'edentates', in part; see also
Manis [scaly ant-eater] and
Orycteropus [aard-vark])
eyeshine in, 241
feeding method of, 209
pupils of, 221

taxonomic position of, 139, 676
spiny: echidnas (monotremes), q.v.
antelopes

cheek stripe in, 546
corpora nigra in, 219
interpupillary distance in, 327
taxonomic position of, 676
anterior segment, 174*
Anthropoidea : monkeys -i- apes -i- man;
Simiae; 'higher' primates, q.v.
area centralis and fovea in, 187, 245
circumcomeal sulcus in, 284, 672, €77
circumlental space in, 284, 681*, 683
color vision in, 515-517, 521
eye movements in, 311
eyeshine in, 230, 233, 241
habits of, 201, 227-228
iris coloration in, 545
lens in, 201, 284
macula lutea of, 181*, 201
myopia, normal occurrence of, in, 273,286
optic axes in, 297
pupil in, 221, 228
retinal circulation in, 201
vision without cortex in, 337
Antilocdpra (mammal: pronghom 'antelope')
color change in, 524
lacrimal gland (lacking) in, 426
visual acuity of, 246
Anura (tailless amphibians: frogs, toads,
hylas etc.)
accommodation and refraction in, 257,
265-268, 266, 272-273, 407,
436, 596-597
adnexa of, 266, 407, 419, 421, 436,
593-594

nictitating membrane, 266, 419, 421,
593-594
and ultra-violet light, 374, 489
area centralis in, 187, 266, 305, 493
brow spot of, 339
canal of Schlemm in, 595-596
chorioid of, 595
ciliary body of, 595-597
circulation of eyeball in, 598
classification of, 135, 593
coloration of eye in, 545-546, 548-549
color vision in, 490-494
cornea of, 594-595

dermal color changes in, 527, 535-539
electroretinography of, 489-492
elevation of eyes in, 443
eye movements of, 305, 312, 595

and swallowing, 305, 594, 601
eye-spots in skin of, 544
eyeshine in, 230, 240
foveolae opticae of, 105
habits of, 145, 150, 200, 203, 223, 368,

407, 418-419, 436, 599-600, 653
iris of, 597-598, 619
lens in, 266, 374, 436
median eyes of, 339
ocular proportions in, 594, 600
optical colors in skin of, 543
optomotor reaction in, 492-493
orbit in, 594

permanently aquatic, 223, 407, 419
protractor lentis muscles of, 272 595, 597
pupils of, 220, 223, 293, 407

movements of, 150, 157-158, 161, 218-

nodules of, 273, 595-596 [219

Purkinje phenomenon in, 493
reaaion to movement by, 344
relationship to urodeles, 593, 601
retina in, 148, 161, 184, 598-600

photomechanical changes of, 148, 150,
rhodopsin in, 1 0 1 , 1 03 [ 1 52

sclera of, 594-595, 602

bone in, 274, 595
swallowing, use of eye in, 305, 594, 601
visual acuity of, 312, 412, 493
visual cells of, 53-56, 54, 55, 59, 176,
200, 572, 598-600, 599, 603

oil-droplets in, 145, 203
visual field of, 293, 299
vitreal vessels of, 598, 653
zonule of, 594, 595, 596
Aotus (mammal: night monkey; —Nycti-
area centralis of, 187, 245 [pithecus)

eyeshine of, 233

nocturnality of, 201, 228, 245, 515
retina of, 616, 685

tapetum lucidum fibrosum of, 233, 241,
245

INDEX AND GLOSSARY

725

taxonomic position of, 233, 245, 517
Aparasphenodon (amphibian: an anuran),

pupil of, 223
apes (see Anthropoidea ) , habits and pupils

of, 228
aphakic space of pupil, 160*, 186, 261
Aphyonus (deep-sea teleost), vestigial eye

of, 397
aplanatic: yielding a flat field (said of

lenses)
Apodemus (mammal: a murid rodent),

color blindness of, 512
Apogon (teleost), stripes crossing eye in 546
Aptenodytes (bird: king penguin), square

pupil of, 221, 226
Apteryx (bird: kiwi)

eye and habits of, 201, 500, 650

pecten of, 650, 656-657

refraction and vision of, 273, 281

retma of, 500

ringwulst of, 648
A pus (bird: a swift)

areje and foveae of, 187-188, 308-309

pecten of, 655

ringwulst of, 647
aquatic aaivity, eye and vision in (see also
amphibious aaivity), 368-417

Taxonomically:

fishes, 368-407, 428-429, 431-436, 449-
454,459-461, 592-593

amphibians, 407, 418-419

chelonians, 422-423

crocodilians, 422, 436

lizards and snakes, 438

birds, 226, 425, 438-442, 644

mammals, 407-410, 442-448, 667, 669, 678
aquatic origin of eye, 369-371
aqueous humor

source of, 371-373, 428-429, 592

supposed coloration of, 191
Aquila (bird: an eagle)

eye of, 643

pecten of, 643, 656

retinal area in, 656

skull and scleral ossicles of, 270
Arabs, 246
Arapaima (largest freshwater teleost), lung

of, 392
arboreal: tree-dwelling or tree-climbing
archer-fish: Toxotes, q.v.
Architeuthis (mollusc: giant squid), as food

of Physeter, 412
Ardois signals, 507
area centralis (see also fovea), 181-182*

accommodation and, 283

distribution of, 184-190, 187 (Table III)

eye movements and, 288, 291, 300-312

organization of, 177, 181-182, 190, 685

within tapetalized region, 243, 245-246

taxonomically:

elasmobranch, 184-185, 243, 245

teleosts, 184, 303-305

amphibians, 187, 266, 305,493

reptiles, 186, 188-189, 305-307, 611,
615, 625
Xantusia, significance of, 625

birds, 187-188, 307-310

mammals, 185, 190, 310-312
area striata, 334-335
argentea, 235-236*

taxonomically:

lampreys, 558

elasmobranchs, 567

holosteans, 574-575

teleosts, 581, 584

cladistians, 589
argentine, 235*
Argyropelecus (deep-sea teleost)

eye of, 213

structure and development of, 400-401,

prcescopic larva of, 405 [405

retina of, 399
arhythmicity (see also habits), 143*

adaptations for, 143-168, 430

basis of, 163-164

ocular proportioning in, 173
Aristotle, 526; illusion of, 326*
Arizona (reptile: a colubrid snake)

pupil of, 168, 221, 225

visual cells of, 63, 638

zonule of, 630
Ascidia (non-vertebrate chordates: sea squirts)

larval eye of, 121-122, 324, 339

eye-origin theories based upon, 121-122
armadillos (mammals; see Xenarthra,

Dasypus)
Arthrodira (extinct fish group), scleral

ossicles in, 380
Artiodactyla (mammals: even-toed 'un-
gulates'), 676*

ciliary processes of, 681

cones of, 688

corpora nigra of, 2 1 9, 679

pectinate ligament in, 680

retinal vessels in, 684
Ascelichthys (teleost: a conid), device for

permitting eye-movement in, 454
Aiio (bird: an owl)

pecten shadows of, 365

spearal responsivity of pupil in, 102, 502
astigmatism, 27*-28

significance of, in seals, 447-448

streamlining of eye and, 380

visual angle and, 287
Astronesthes (deep-sea teleost), photophores
of. 402

726

INDEX AND GLOSSARY

Astroscopus (teleost: a stargazer), dorsal
binocular field, elertric organ, and
oculorotatory muscles of, 293
atavisms: re-appearances of charaaeristics of

remote ancestors; 37-38, 464
Ateleus (mammal: spider monkey), color

vision of, 515, 517
Atelopus (amphibian: an anuran), possi-
bility of yellow filters in, 599
Athene (bird: an owl)

spectral responsivity of pupil in, 501
white lids of, 546
Atherina (teleost: silverside), color vision
and brightness discrimination of,
476-477
Atractaspis (reptile: a viperid snake)
habits of, 640
pupil of, 221, 225, 640
atropin, 157
Atsatt, 540-541
auks

accommodation in 440
Crampton's muscle in, 441
habits of, 439-440
nictitans-lens in, 440
auroral: active in morning twilight (c/.

crepuscular)
Austrolethops (teleost: a goby), degenerate

eye of, 210
autokinetic phenomenon, 347*
autonomomimetic: said of drugs which sim-
ulate the actions of the autonomic
(sympathetic + parasympathetic)
nervous system
avahi: Lichanotus, q.y.
avascular: devoid of blood vessels
aviation and vision, 77
aye-aye: a low primate; 139
Azara (mammal: an opossum), pure-rod (?)
retina of, 675

Babak, 535, 692 (entry for p. 527)

law of, 527
baboons

color vision of, 515

normal myopia of, 273, 286
Bailey, 499
Balcenoptera (mammal: great blue whale),

eye of, 413, 677
Balaton, Lake, 210, 236
Balfour, eye-origin theory of, 121, 122, 123,

126, 128
Balistapus (teleost: a triggerfish), fovea in,

304
Balisles (teleost: a triggerfish), fovea in, 304
Ballowitz, 529
banded gecko: Coleonyx, q.v.

Barathronus (deep-sea teleost), vestigial eye
Barbatula (teleost) [of, 397

color vision of, 472-473

dermal color changes of, 526-527
barbels: sensory 'whiskers' of catfishes etc.
barrel distortion, 354*
Barrett, 302, 318

Basiliscus (reptile: an iguanid lizard), visual
basking [fields of, 294

habit of, (see habits)

-shark: Selache, q.v.
bass

rock: Ambloplites, q.v.

spotted: Micropterus, q.v.

true (sea-), see Serranidae
batensoda: Synodontis, q.v.
batfishes (teleosts, near anglers; see also
Halieutichthyes, Lophiomus,
Ogcocephalus)

falciform process (lacking) in, 583

vitreal vessls in, 582-583
bathopsis: perception of depth; 315*
bathybic fishes (see deep-sea fishes)
Bathyergidae (mammals: mole-rats), eyes of,
Bathylagus (cleep-sea teleost) [677

enlarged eye of, 395

stalk-eyed larva of, 405
bathypelagic fishes (see deep-sea fishes)
Bathytroctes (deep-sea teleost)

ocular shape in, 402

rod fovea of, 187, 190, 402
Batoidei (elasmobranchs: skates and rays)

accommodation and refraction in, 251,
260, 265-267, 272-273, 381, 429

chorioid of, 243, 566

ciliary body of, 372, 567

embryonic fissure (open) in, 265
folds of, 262

cornea of, 566

deep-sea, 392, 394, 397-398, 405

distribution of, 563

dorsal position of eyes in, 385

eye movements in, 303, 386, 429, 452,
692 (entry for p. 452)

habits of, 200, 222, 303, 385-386, 429,

iris of, 567, 575 [563, 568

lens of, 200, 567

oculorotatory muscles in, 303, 692 (entry

optic nerve of, 569 [for p. 452)

optic pedicel of, 564-565, 578

orbit of, 452, 564-565

pupil (and operculum) of, 150, 155, 158-

159, 220, 222, 224-225, 256, 273,

consensual reflex of, 158 [386

retina in, 568

'ramp' attitude of, 255

sclera of, 563

shape of eye in, 255, 565-566

INDEX AND GLOSSARY

727

size of eye in, 386, 563

tapetum lucidum of, 243

taxonomic position of, 135-136

temporary lids in, 386, 432, 452

tenacular ligament of eyeball in, 578

visual cells of, 568, 688

visual fields of, 293, 385-386

zonule of, 260, 268, 372, 429, 567
bats: Chiroptera, q.y.
Bauer, 474, 476-479
beaded lizards: Heloderma, q.v.
bears

blink (false) in, 427

eyes of, 145, 245

habits of, 145, 170, 443

nictitating membrane of, 426-427

psychic weeping in, 41

retinal degeneration in, 228

tapetum lucidum in, 145, 245

white ('polar"), 245, 426-427, 443
beavers: Castor, q.v.
Beebe, 349, 373, 396, 404, 528
Beer, 283, 287, 415, 438, 587, 614
Belong (teleost: needlefish)

accommodation in, 582

falciform process of, 582

pigmented cornea of, 219, 433
beluga: white whale (Delphinapterus) , 412
Bengalichthys (deef>-sea elasmobranch),

vestigial eye of, 397
Beniuc, 364-365, 489
Benner, 341
Benoit, 128

Benthobat'ts (deep-sea elasmobranch), de-
generate eye of, 397, 563
benthonic fishes: deep-sea fishes, in part;
benthos, 384* [speaacles in, 461

of deep seas, 392*
eyelessness in, 397-398
Bentley, 473
Belt a (teleost: Siamese fighting-fish)

biological moment of, 364-365

color vision of, 364-365, 489
Bierens de Haan, 515, 521
bifocal lenses, 257, 332-333, 440-441
bile salts, 75
binocular vision (see also visual fields); 313-

acuity of, 308, 331-333 [338

arecB centrales, foveae, and, 300-312

in birds, 307-310, 309, 320, 323-324, 327,

brightness in, 331-332 [331, 643, 651

of colors, 90-91, 325, 333-338, 335

in deep-sea fishes, 402-403

evolution of, 326-331

eye movements and, 300-312, 386

in monotremes, 666, 669

position of eyes and, 290-291 , 311, 385-386

transversalis muscle and, 269

biological moment (see moment)
bioluminescence (see also photophores), 396*
bird snake, African: Thelotornis, q.v.
birds

accommodation and refraction in, 251,
257, 269-282, 438-442, 441,
647-648
adnexa in, 118, 419-425, 420-421, 440,

641-642, 644
amphibious, adaptations of, 438-442
area and fovea of, 182-183, 187-189, 195,
307-310, 308-309, 324, 442, 659,
661-662, 692 (entries for pp. 187,
195)
binocularity in, 307-310, 309, 320, 323-

324, 327, 331, 643
blinking, act of, in, 644
canal of Schlemm in, 646
chorioid of, 644-646

muscle cells in, 273, 281, 442, 645
ciliary body in, 118, 277-281, 280, 441,

645-646, 680
color vision of, 191-193, 196, 466, 497-
comeaof,441,641,644 [504,519-520
eye movements of, 213, 307-310, 329
eyeshine and tapetum (?) in, 230, 240,
Gemminger's ossicle of, 643-644 [646

habits of, 150, 169-170, 176, 201, 203,
205-209, 307-310, 324, 341-342,
344-345, 438-442, 655-659
iris of, 269, 441, 647

coloration of, 545-551
lens in, 118, 276-277, 441, 642-643,

645, 647-648
monocular stereopsis in, 341-342
movement, perception of, by, 344-345,

354, 365-367
nasad asymmetry of, 643
ocular proportions in, 172-174, 212-213,

641-643, 665-666
ocular resemblance to lizards, 641, 689
optic nerve in
chiasma of, 47
head of, 179-180
orbit of, 642
origin and relationships of, 134-135, 139,

203, 641
origin of ocular plan of, 622
pecten of, and its significance, 118, 180,

188, 308, 365, 648-659, 643, 649
photosensory ependymal cells of, 79, 127-
pupils of, 221, 226, 439-440 [128

consensual reflex of, 158
movements of, 150, 156, 162, 226, 269
spectral responsivity of, 102
retina in, 50, 178, 196, 659-662, 660, 684
photomechanical changes of, 150, 156,
rotatability of head in, 213 [162

728

INDEX AND GLOSSARY

birds — cont'd

sclera in, 441, 642-644

ossicles of, 270-271, 274, 280, 441,
643-644

visual acuity of, 169-170, 172-174, 206-
209, 216, 307-310, 642, 661-662
compared with human, 661-662, 689

visual cells of, 54, 176, 195, 215-216, 588,
611, 621, 660-661, 675, 692 (en-
try for p. 195)
oil-droplets of, 102, 191-193, 196-197,
201,203

visual fields of, 289-291, 295-296, 300,
307-319, 309, 320, 323
Birukow, 492-494
Bit is (reptile: a viperid snake)

binocular field of, 294

visual cells of, 639-640

zonule of, 630
bitterns

area; and fovea of, 187, 307

freezing pxasture of, 296, 309

visual fields of, 296
Black, 312

black skimmer: Rynchops, q.v.
blackbird. Brewer's: Euphagus, q.v.
blackfish: Centra pristes, q.v.
BlSsser, 498
blennies

accommodation in, 261, 272

amphibious habits in, 431-434

dorsal binocular field in, 293

falciform process of, 582
Blennius (teleost: blenny)

accommodation in, 261

fixation by, 324

fovea in, 304

visual-cell mosaic in, 587
Blessig, cysts of, 10
Blicca (teleost), retinal tapetum lucidum of,

236
Bliccopsis (teleost), retinal tapetum lucidum

of, 692 (entry for p. 236)
blind spot (see scotoma)
blinking reflex (see lids)
blue shark: Prionace, q.v.
blue-blindness 99*
bluegill sunfish: Lepomis, q.v.
boas: Boidee (in part), q.v.
Boida (reptiles: boa -t- python family)

canal of Schlemm in, 629-630

fossorial, spectacles of, 450

habits of, 201

legs in, 138

lens in, 630

pupil in, 220, 225

retina in, 167, 636, 689

sclera in, 627

visual cells of, 61, 636, 689

vitreal vessels of, 654
Boleophthalmus (teleost: mud-skipper), eyes

and habits of, 431-432
Boll, 74, 100

Bombina (amphibian: fire-bellied toad),
bones [pupil of, 161, 223-224

circumorbital, 271, 274, 381

conjunctival, 569

of sclera (see sclera, ossicular ring of;
Gemminger)
boobies: Morus, Sula, qq.v.
Bornemeier, 510
borzoi, visual hunting by, 345
Bos (mammal: domestic cattle)

color vision in, 466, 505

interpupillary distance of, 327

optic axes in, 297

rhodopsin of, 373

tapetum lucidum of, 232

taxonomic position of, 676

visual field of, 298
Bothida (teleosts: left-handed flounders),
sessile eyes and pupillary opercula
of, 386
bottom fishes, adaptations of, 384-387, 453
Boveri, eye-origin theory of, 125-126, 128
bower-birds, color-interest of, 466
bowfin: Amia, q.v.

Bowman, membrane of, 8, 644, 667, 672, 678
Box (teleost)

binocular field of, 292

color vision of, 476-478
box turtle: Testudo, q.v.
Brachycephalida (amphibians: an anuran fam-
ily), oil-droplets in (?), 599-600
brain, visual involvements and structures of

(see visual pathway, central); 5
Brauer, 403

bream, European: Abramis, q.v.
Brecher, 515

Brevicipitidae (amphibians: an anuran fam-
ily), pupils in, 223
brightness: subjective connotation of photic
energy or intensity, q.v.; 80*

binocular, 331-332

constancy of, 530-531

discrimination of, 471-472, 487

distinctness of, from saturation, 84-85, 96

enhancement of, by tapetum lucidum, 230

indicated by pupil, 500

reference of, to intensity, 247

spectral distribution of, 76, 87', 96, 101-

Purkinje phenomenon and, 87-88 [ 1 02
Brotulida (teleosts)

blindness in, 388, 399

habits and distribution of, 388

spectacles in, 450

INDEX AND GLOSSARY

729

Brown, F. A., 528
Brown, R. H., 511-512
Briicke, 235, 279-280

muscle of, 10, 33*, 280-281, 441, 437,
583-584, 646, 673
distribution of, 272-273 (Table VIII)
Bubo (bird: an owl)

color change of iris in, 550-551

eye of, 213, 425, 643

nictitans tendon of, 425

pecten in, 643, 656

photopic visual acuity of, 216

retinal area in, 656

retinal summation in, 661
von Buddenbrock, 492-493
budgerigar: Melopsittacus, q.v.
Bufo (amphibian: common toad)

iris folds of, 596

scleral cartilage of, 595
Bufonida (amphibians: toad family)

accommodation in, 436

aquatic, spectacle in, 593-594

habits of, 436

taxonomic position of, 593

visual cells in, 598-599
Bull, 487-488
bullets, visibility of, 351
bullhead: Ameiurus, q.v.
Bumpus, 524
Bungarus (reptile: an elapid snake)

pupil of, 221, 225

visual cells of, 638
Burford, 506, 513

Burhinus (bird: stone-curlew), eyes, habits,
Burkamp, 480 [and pecten of, 657

Burkhardt, 603

burrowing habit (see habits, fossorial)
bush-baby: Galago, q.v.
Butcher, 532
Buteo (bird: a hawk; European 'buzzards')

electroretinography of, 500

fovea of, 182-183

concentration of cones in, 661

pecten of, 649
shadows of, 365

retina of, 659

visual acuity of, 661
butterfly-fish: Pantodon, q.v.
buzzard (see Buteo)

Cabrita (reptile: a lacertid lizard), lid

window of, 450
Oecilia (amphibians: 'blind-worms')

eye and tentacle in, 605-606, 635

pupils of, 220, 223, 606

retina in, 216,636,692 (entry for p. 150)

taxonomy of, 135, 593, 605

Ccecilid (amphibian: a cacilian), lack of

eye muscle in, 606
Caiman (reptile: a crocodilian)
eyeshine of, 231
lids of, 422
visual fields of, 294
Calamoichthys (cladistian), 589
accommodation (?) in, 263
habitat of, 588
relationships of, 136
Callicebus (mammal: a cebid monkey),

color-vision of, 517
Callithrix {-Hapale, q.v.), cone: rod ratio

in, 686
Callosaurus (reptile: an iguanid lizard),
dermal color changes in, 540-541
Calypte (a hummingbird), fundus of, 188
Calyptocephalus (amphibian: an anuran),
pupil of, 223; 692 (entry for
p. 223)
camels (= Tylopoda, in part; see also drom-
lid movements in, 425 [edary)

pupils of, 219, 256

corpora nigra of, 219, 227
tapetum lucidum in, 241
taxonomic position of, 241
camera (and photography) compared with
eye (and vision), 6, 66, 68, 229-
230, 254, 366-367, 395, 448, 462,
camouflage (see also color changes) [503
in animals, 341, 544
detection of, with filters, 196
campanula Halleri (see muscle, retractor

lentis)
canary, color- feeding of, 524
CanidcB (mammals: dogs, foxes, wolves etc.,

qq.v.), optic axes of, 297
canthi (of lids), 38*-40, 423
Caprimulgus (bird: European goatsucker),

pecten of, 656
Caranx (teleost: a scombrid), adipose lids
Carassius (teleost: goldfish) [in, 382

cornea of, 579
degeneration of eyes in, 390
pigment epithelium of, 44
rhodopsin of, 103
'telescope' variety of, 263
visual cells of, 54-55, 586
Carcharodon (elasmobranch: man-eating
shark ) , eye and accommodation
of, 259
Carnivora (order of mammals; flesh-eaters)
accommodation in, 681
area centrales of, 185, 187, 245
ciliary body in, 285, 679, 681-683
color vision in, 505-508
corneal curvature of, 211-212, 677
eye movements in, 311

730

INDEX AND GLOSSARY

Carnivora — cont'd

frontality of, 290, 297

habits of, 145, 170, 176, 204, 209, 504

iris in, 684

lack of filters in, 203-204

lens in, 684

nasad asymmetry of, 173, 300, 678-679

nictitating membrane in, 426-427

ocular proportions in, 173

optic axes of, 297

pectinate ligament in, 680

pupil in, 221, 245

retina! image size in, 176, 245

retinal vessels in, 654, 684

significance of motion for, 344

size of eye in, 145, 176, 245, 677

tapetum lucidum in, 145, 232-233, 234,

241, 244-246
taxonomic position of, 139, 676
visual ceils of, 685, 688
visual fields of, 296-298
weapons of, 209
zonule in, 681-683
carotene (a carotenoid, ^.v.)
carotenoids: hydrocarbon pigments of plants
and animals; 192, 198, 202, 204,
carp: Cyprinus, q.v. [524,526,534

Carrick, 524
caruncle, 38-40^^ 39
cassowary: Casuarius, q.v.
Castor (mammal: beaver)
ciliary processes in, 681
eyes and vision of, 443-444
habits of, 201, 443
optic axes of, 296-297, 443
Casuarius (bird: cassowary), pecten and

habits of, 656-657
catadromous: said of fishes which live in
fresh water but breed in the sea;
cataract, 21* [372

extraction, vision after, 29, 204
vision in, 99
Catarrhina (mammals: Old-World anthro-
poids), taxonomy and color vision
in, 516-517, 521
catfishes (see siluroids)
cats (Felidce)
domestic

accommodation of, 287, 681-683

anterior segment of, 681-683

ciliary body of, 286, 683

color vision in, 338, 506-507, 521

cones of, 215

convergence in, 312

cooperation of lids and pupil in, 428

cornea, relative size of, 289, 298

critical fusion frequency of, 354

electroretinography of, 521

eyeshine of, 233-234

habits of, 215, 219

haw (nictitating membrane) of, 426

iris coloration in, 543, 548, 550

lateral geniculate body of, 338

ocular and image sizes in, 210

optic chiasma of, 319

pigment epithelium of, 56

pupil and iris muscles of, 2 1 8, 227,

256, 501
retinal and cortical resolving power in,
retrartor bulbi muscle of, 420 [207

scotopic vision of, 215
Siamese, blue iris of, 543
spectral sensitivity of, 501
surgical interchange of eye muscles in,
tapetum lucidum of, 234-235 [311

visual acuity of, 207
visual field of, 289, 298
zonule of, 683
habits of, 173,227
iris coloration in, 545
ocular proportions in, 172-173
optic axes in, 297
pupils of, 162, 227
visual acuity in, 172
visual fields of, 296-297
cattle: Bos, q.v.
caudad: toward the tail
Causus (reptile: a viperid snake)
pupil of, 221, 225, 640
visual cells of, 639-640
cavemicolous (cave-dwelling) vertebrates,

209-210, 300, 376, 387-390, 396,
600, 603
evolution of, 387-390, 399
retention of eyes by, 387, 390
skin of

depigmentation, 533
photosensitivity, 128
speaacles in, 450, 453
cayman: Caiman, q.v.
Cebidae (mammals: an anthropoid family),

color vision in, 516-517
Cebus (mammal: capuchin monkey)
color vision of, 516-517
visual acuity of, 207
Cemophora (reptile: a colubrid snake),

visual cells and habits of, 63, 165-
166, 637-638
Centrarchida (teleosts: sunfishes and fresh-
water 'basses'), red iris in, 549-551
Centropristes (teleost: a serranid; blackfish),
eye-movements, pupil, and possible
fovea of, 304-305
Cephaloptera (elasmobranch: a ray), pupil

of, 220, 222
Cepola (teleost), binocular field of, 292

INDEX AND GLOSSARY

731

Cepphus (bird: pigeon guillemot), fundus

of, 188
Cerastes (reptile: a viperid snake)

spectacle of, 450

visual cells of, 640
Cerberus (reptile: a homalopsine snake),

eye and habits of, 293, 295
Cercocebus (mammal: mangabey monkey)

color vision of, 515

fovea of, 190

number and length of cones in, 190, 686
Cereopsis (bird: a goose), ringwulst and
Cermak, 359 [pecten in, 648, 656

Cervidae (mammals: deer family)

interpupillary distance in, 327

multiple optic papillae in, 367

oDtic axes in, 297

taxonomic position of, 676
di Cesnola, 524

Cetacea (mammals: whales, q.v.)
Cetomimus (deep-sea teleost), vestigial eye

in, 398
Chalcides (reptile: a scincid lizard)

binocular field of, 294

lid window of, 450
Chamaleo (reptile: a chameleon; see Cham-
chameleons [ aleontidae )

Florida: Anolis, q.v.

true: Chamaleontidee, q.v.
ChamaleontidsB (reptiles: a lizard family)

accommodation in, 270

adnexa in, 423

conus papillaris in, 653, 658

dermal color changes in, 494, 526, 528,

eye of, 173, 423 [538-539

eye movements in, 306, 311, 320

fovea in, 173,306,623
concentration of cones in, 625

macula lutea (?) in, 200, 203

optic chiasma in, 320

ringwulst of, 1 73, 624

scleral cartilage of, 623

scleral ossicles in, 274

slow movements of, 270, 306, 653, 658

visual field in, 306
chamois (mammal: an antelope); interpupil-
lary distance of, 327
Chanos (teleost: near herring), cornea and

spectacle in, 450, 460
characins (teleost family Characinidce), lack
of chorioid gland, pseudobranch
in, 581
Charax (teleost), color vision of, ^76A77
Charina (reptile: rubber boa)

canal of Schlemm in, 629-630

ciliary body of, 629

fibrous tunic of, 628

lens of, 630

Chase, 102

Chelmon (teleost), 'eye-spots' on body of,
Chelodina (reptile: Murray turtle) [544
lens of, 669

lid window of, 450, 457-458
optic axes of, 294
Chelonia (turtles, tortoises, terrapins)
accommodation and refraction in, 251,

273-279, 436-438, 437, 609-610
adnexa in, 421-423, 428, 450, 457-458,

547
amphibious, adaptations of, 436-438
area centralis and fovea in, 184, 186-187,
chorioidin, 609, 611 [190,305,611

ciliary body in, 277, 437, 609-610, 623
color vision in, 494-496, 519
coloration of eye and body in, 546-547,

550
conus papillaris in, 611, 653, 657-658
cornea in, 609

departure from standard reptilian pattern,
eye movements in, 305 [622

eyes of, 547, 608-612, 609
habits of, 161, 197-198, 200, 216, 224,

437-438, 450, 494, 608, 653
iris in, 609-610
lens in, 610

ringwulst of, 609-610
median eyes (lacking) in, 340
ocular proportions in, 609
optic axes of, 294, 296
pupil in, 150, 220, 224, 437
retina in, 161, 177, 224, 437, 611-612,

623, 653
photomechanical changes of, 150, 161
sclera in, 609

ossicles of, 274, 417
significance of motion for, 270, 344
taxonomy and distribution of, 135, 138,
transparency of media in, 438, 609 [608
transversalis muscle in, 279, 610
visual cells in, 59, 150, 161, 176, 216,

611-612, 621, 653, 661
oiWroplets of, 102, 192-193, 197-198,

200, 202, 661
zapfensubstanz of, 495
visual fields of, 293-294, 296
vitreous in, 610-611
Chelonia (reptile: a sea turtle)
embryonic conus papillaris of, 611
optic axes of, 296
Chelydra (reptile: snapping turtle)
binocular field of, 293-294
embryonic conus papillaris of, 611
eye closure in, 427
retina of, 612

sensory guidance of, 437-438
visual cells of, 54, 216, 612

732

INDEX AND GLOSSARY

chiasma, optic (see optic chiasma)
chicken: G alius, q.v.
Chimcera (elasmobranch: a chimaera)
oculorotatory muscles of, 564, 574
retina of, 568
chimaras: Holocephali, q.v.
chimpanzee

color vision of, 515
visual acuity of, 207
Chironectes (mammal: water opossum),

443, 664
Chiroptera (order of mammals; bats; := Micro-
chiroptera + Megachiroptera, qq.v.)
binocularity in, 310
cornea: retinal areal ratio in, 289
diurnal 'blindness' of, 168
feeding method of, 169
lens shape in, 213
localization by, 343

mammillated chorioid in, 254-255, 270,
optic axes of, 297 [273, 678

pupil in, 162, 221
retina in, 216, 254-255, 273, 685
degeneration of, 228
exception to avascularity of, 684
tapetum lucidum in, 238, 241, 684
size of eye in, 677
taxonomic position of, 139, 676
upward tilt of eyes in, 296
use of caves by, 209
visual cells of, 216, 685
ChloTophthalmus (teleost), keyhole-shaped

pupil of, 292
chlorophyll, spectrum of, 196
Cholapus (mammal: two-toed sloth), pupil

of, 221, 228, 257
Chologaster (teleost: an amblyopsid), eyes

and habitat of, 387
chondrocranium: the primitive cartilaginous

vertebrate brain-case; 557
Chondrostei, 135-136*, 569*

eyes of, 569-573, sub-index p. 569
primitive, visual cells of, 591, 600, 612,
relationships of, 589 [688

chordates: Chordata (a phylum of animals
having dorsal, tubular nervous sys-
tems, notochord, and gill-slits at
some period in the life-cycle; in-
cludes vertebrates and also Ascidia,
Amphioxus, etc. - qq.v.)
early, habits of, 208
chorioid, 13*

choriocapillaris layer of, 8, 14, 51*
function of, 51, 652
ontogenetic disappearance of, 672
and tapetum lucidum, 231-232, 234,
endothelial cells of, 234 [654, 672

function of, 13, 625, 652

'gland' of, 118, 261, 365, 574*, 577, 581-
582, 651

mammillation of, 254-255, 678

muscle cells in, 273, 281, 442, 645

pigmentation of, function of, 13, 228-229

suprachorioidea of, 566*
elasmobranchs, 566
sturgeons, 570-571

taxonomically:

lampreys, 558

elasmobranchs, 566

sturgeons, 570-571

holosteans, 574

teleosts, 581-584

cladistians, 589

dipnoans, 590

anurans, 595, 598, 602

urodeles, 602

Ccedlians, 606

chelonians, 609, 611

crocodilians, 613

Sphenodon, 617

lizards, 617, 623

snakes, 629

birds, 644-646

monotremes, 668

marsupials, 672

placentals, 678

man, 6-8, 13-14, 678
chroma, 85* -86
chromatic aberration, 82, 193*- 1 94

compensations for, 193-195
chromatophores, 525, 525*-526, 584

endocrine control of, 529, 550

innervation of, 529, 540
chromophore, 75*

chronoscope: precision instrument for meas-
uring minute intervals of time; 356
Chrosomus (teleost; a dace), dermal color

changes in, 525
Chrysemys (reptile: painted turtle)

area centralis of, 1 86

coloration of eye and head in, 546-547

double cone of, 59

embryonic conus papillaris of, 611
Chrysochloris (mammal: golden mole)

eyes of, 677

taxonomic position of, 676
Chrysopelea (reptile: flying-snake), optic

axes of, 294
Chrysophrys (teleost), iris-angle region of,

159
chunk-head snakes: Amblycephalidee, q.v.
cichlids (teleost family Cichlidje), dermal

color changes in, 525
ciliary body (see also accommodation,
muscles)

asymmetry in, 300, 442

INDEX AND GLOSSARY

733

folds of (not processes; cf. ciliary proc-
esses), 259, 276*, 372, 429, 435,
567, 571, 681-683
relation of, to lens

taxonomically:

fishes and amphibians, 417, 592-593

reptiles, 275, 277, 284, 607, 632-633

birds, 441-442, 645-646

monotremes, 284

marsupials, 284, 674

placentals, 284, 681-683
secretory function of, 14, 276, 286, 371-

373, 408-409, 418
taxonomically:
elasmobranchs, 564, 567
sturgeons, 571
teleosts, 580, 583-584
anurans, 595-597
urodeles, 602
chelonians, 275, 610
crocodilians, 613
Sphenodon, 618-619
lizards, 623-624
snakes, 629-630, 673
birds, 442, 642, 645-646
monotremes, 667^668
marsupials, 673-674
placentals, 286, 300, 408-409, 678-683

man, 13, 14, 15,16,32-33,36,682-683
ciliary processes, 13*, 14-15, 31, 115-116,
276*, 681*
as anchorage for dilatator, 447
invention and funaion of, 276, 418, 653
surgical excision of, 651
taxonomically:
amphibians, 267, 595-597, 602, 605
sauropsidans, 276-277

chelonians, 277, 437, 610

crocodilians, 613-614

birds, 643, 645-646, 648, 651, 680
mammals, 284, 667-668, 673, 679-683

seals, 445-446

sirenians, 409

structural types in, 286, 681

vestigial status of, 286
ciliary web, 667, 668*, 669, 673, 681
circulation of eyeball (see also 648-659 for
nutritional significance)
taxonomically:
lampreys, 558

elasmobranchs, 566-567, 571
sturgeons, 571, 598
holosteans, 575, 598
teleosts, 581-583, 598
anurans, 598, 602, 611
urodeles, 602
chelonians, 61 1
Sphenodon, 619

snakes, 630-631

birds, 644-659

mammals, 531, 672, 684
man, 13, 14-15, 16,51
circumlental space, 681*-683
Circus (bird: a hawk)

single cone of, 54

retina of, 659
Citellus (souslik, ground-squirrel; see
squirrels, ground-), 514-515
Cladistia (Calamoichthys + Polypterus,

eyes of, 589 [qq.v.), 136*

habits of, 150, 200, 588

pupils of, 220

retinal and visual cells of, 692 (entry for
p. 589)
Clarias (teleost: a catfish), visual cells in,
Clemmys (reptile: a terrapin) [586

binocular field of, 294

color vision in, 494-495

stripes crossing eye of, 546
Clethrionomys (mammal: red-backed mouse),

color vision in, 512-513
climbing perch: Anabas, q.r.
clingfishes (teleost family Gobiesocidae),

falciform process in, 582
clivus (of fovea), 188*, 190
Cloquet, canal of

caecilians, 606

chelonians, 609, 611

man, 7, 114*, 114
Clupea (teleost: herring), adipose lids of,

383
Clupeidae: herring family; see clupeoids
clupeoids (teleosts: herrings and their allies)

adipose lids of, 383-384, 460-461
spectacle made from, 460

falciform process in, 582

relationships of, 386

scleral ossicles in, 579
coal titmouse: Parus, q.v.
Cobitis (teleost: a loach), spectacle of, 450
cobras: Elapidae (in part), q.v.
codfishes: Gadus, q.v.
Coenolestes, 664*
Colaptes (bird: flicker)

chorioid of, 645-646

Gemminger's ossicle (lacking) in, 643

retina of, 659
colchicine: a drug which halts dividing cells
and thus reveals their abundance
in a tissue; 109
Cole, 507

Coleman, 499, 509
Coteonyx (reptile: a eublepharid lizard)

ciliary muscle of, 624

cornea of, 623

dermal color changes of, 541

734

INDEX AND GLOSSARY

Coleonyx — cont'd
lids of, 623

'lashes' of, 424
slit pupil of, 168
visual acuity of, 168
visual cells of, 62, 168, 626-627
collared lizard: Crotaphytus, q.v.
Collins, 509
color, 81-84*

aberration of (see chromatic aberration)
chroma of, 85-86*
complementary, 83* -84

in birds, 499

in fishes, 364-365, 489

in hemianopia, 336
constancy of, 247
-contrast, 498-499
differential absorption and, 103
discrimination of, 92-93

in anomalous trichromasy, 97

in dichromasy, 97
of eye (see iris, coloration of)
of eyeshine, 231
'fatigue' for, 93, 96
-filters (see color-filters)
of flowers, and color vision, 503-504
vs form (associations), 489-490
mixture of, 83-84, 463, 471-472, 489

binocular, 90-91, 325, 333-338, 335
optical, 525, 543
pairs, disappearing, 84*
photomechanical changes and, 152
-poverty (see color blindness)
primary, 83-84*

in dichromasy, 97
printing of, 88
refractive error for, 194
spectral location of, 92, 94
-weakness (see color blindness)
white valence of, 86-87*
words for, 521
color blindness (see also color vision)
anomalous trichromasy, 97*
as 'atavism', 464

dichromatic (='Daltonism'), 97-100*, 466,
470, 692 (entry for p. 99)

normal for a species, 470, 516-517
total, 92, 96-97*, 470, 474

physiological (of periphery), 475
color cells (of brain), 522-523
color changes

as empirical evidence for color vision, 466

in internal organs, 528-529

in iris (see iris, coloration of)

'morphological', 527*, 528-532, 535-543

'physiological', 527*, 532-536

m skin of body, taxonomically:

fishes, 479-483, 523-538, 525

amphibians, 527, 535-537, 539
crocodilians, 542-543
lizards, 524-526, 536, 538-543
snakes, 526, 542-543
birds, 524-525
mammals, 524
color circle, 82-83*, 471, 480, 488, 500
color-filters

action and use of, 81-82, 85, 469, 483-484

effert of, on contrast, 195-196

intra-ocular, 191-205,200-201 (Table IV)

Noviol, 199

of U. S. Navy, 198
color vision (see also color blindness), 81-

angling and, 472 [103,462*

cataract and, 99, 204

cerebral locus of, 337-338, 521-523

and color-filters, 191-198

dichromatic (see color blindness)

distribution of, 64-65, 518-521, 519, 588

diurnality and, 464, 504-505, 518-521

evidence for, 465-472

evolution of, 53, 65, 464-465, 518-521,
519, 688-689

flash-frequency and, 355

flower colors and, 503-504

hue discrimination in, 471, 487* -488

investigation of, 65, 467-472

monochromatic (see color blindness, total)

optomotor reartion and, 302

peripheral, 89, 355

photochemistry of, 75, 100-103

in senescence, 199

theories of, 75, 89

trichromatic, mechanism of, 88-96, 94, 464

value and origin of, 164,462-465, 518-521

visual acuity and, 464

visual-cell transmutation and, 63, 464-465,

taxonomically: [520,688-689

fishes, 364-365, 467, 472-490

amphibians, 490-494

chelonians, 494-495

crocodilians, 496

Sphenodon, 497

lizards, 465, 495-496

snakes, 465, 497

birds, 497-504

mammals, 465, 467-472, 504-518, 688-689

coloration, protective (see also iris, coloration

of; color changes), 466, 523-524,

colored papers, 470-471 [543-551

Bradley's, 507

Hering's, 496

Nendel's, 506
Coluber (reptile: a colubrid snake)

accommodation in, 456

visual cells of, 166

visual fields in, 294

INDEX AND GLOSSARY

735

Colubridae (reptiles: central snake family)
canal of Schlemm in, 629-630
derivatives of (see Elapidae, ViperidcB,

Crotalids), 629
fossorial, spectacles of, 450
habits in, 201
pupil in, 221, 225
retina in, 61, 167
visual cells in, 63, 165-166, 201, 636-640,

637-639
vitreal vessels of, 654
yellow lens in, 201
Columba (bird: domestic pigeon), 173
accommodation and refraction of, 281-282
area centralis and fovea of, 187, 190
blinking act in, 644
color vision of, 499, 501
cornea: retina areal ratio in, 289
critical fusion frequency for, 354
head movements of, 342
oil-droplet fields of, 196, 499, 503
opacity of media to ultra-violet, 196
pecten shadows of, 365
pupil reflexes of, 158, 500-501
retina of, 659
visual acuity of, 207
visual fields of, 295
Colvin, 506, 513
commencement point, 252*, 252
commensal: an organism which depends for
food upon another organism, but
does the latter no harm; see para-
site, Encheliophis, Typhlogobius
conditioned reflex: a response made to stim-
ulus B, after stimuli A and B have
been repeatedly presented together
— stimulus A being one to which
the response is spontaneously made
by the species in question; 486,
488, 491, 494
conjugation of eyes (see eye-movements of
mammals, binocular vision
[evolution of] )
conjunctiva, 10-11*, 382, 570
bones in, 569

folds of, serving as lids, 427
origin and homologies of, 11, 449-453,

451
simulation of lid by, 387
Connolly, 481

Constrictor (reptile: common boa)
canal of Schlemm (lacking) in, 629
ciliary body of, 629
visual fields of, 294
contaa lens: a type of corrective spertacle
which snugly fits the eyeball; 441
contrast

color-. 498-499

enhancement of

by color vision, 463-464
by intra-ocular color-filters, 195, 502-503
conus papillaris, 607* (see also 648-659 for
functional significance)

taxonomically:

chelonians, 611, 658

crocodilians, 615

Sphenodon, 620

lizards, 611, 624-625, 632, 658

snakes, 631, 633

mammals, 670, 672
convergence (see accommodation, converg-
coots [ence and)

feeding habits of, 439

head movements of, 342
copperhead: Agkistrodon, q.v.
coral snakes (Elapidaj, in part), visual cells
cormorant: Thalacrocora^, q.v. [in, 638

cornea (see also Descemet)

accommodation of, 278, 281, 441

asymmetric pressure on, 379-381

autochthonous layer of, 577, 580*

history of, 436, 449-453, 451, 579-580,
667

optical elimination of (by water), 264-
265, 290, 380, 417, 441-442,
444, 448, 592
compensations for, 430, 434-436, 438,
440, 442, 446

osmosis through, 369-373, 592

peculiar laminations of, 580, 590

pigmentation of, 219, 433-434
yellow, 191, 200, 202

size of, 211-212, 214, 377, 408, 424, 441,

support of, 416-417 [444-446,667,671

surface of, 417, 578

thick, 441, 443

vascular, 602, 678

visual angle and, 289, 377

wool on, 453

taxonomically:

lampreys, 557

elasmobranchs, 219, 566

sturgeons, 569-570

holosteans, 200, 574

teleosts, 200, 219, 574, 577, 578-581, 667
cleavage of, 451, 453, 579-580

dipnoans, 590

amphibians, 592-595, 601, 606

chelonians, 609

crocodilians, 613

Sphenodon, 617, 623

lizards, 617, 623

snakes, 627

birds, 641, 644

monotremes, 666-668, 667

marsupials, 671-672

736

INDEX AND GLOSSARY

cornea — cont'd

placentals, 677-678

cornification in, 412, 445, 665, 678
man, 6-8, 9, 10-12, 27-28, 29-30, 38,
sirenians, 408-409 [40-41

whales, 412-414, 413, 416
Corona, 535

Coronella (reptile: a colubrid snake), zonule
corpora nigra (see pupil) [of, 630

corresponding points 317*-318, 322, 329-331
cortex, cerebral (visual), 329, 334-335

resolving power of, 207
Corydoras (teleost: a catfish), eye and false

blink of, 303, 387
Coryphanoidida (teleosts: grenadiers)
as ancestors of cods, 398-399, 586
eyes of, 398
Coryphopterus (teleost), internal coloration

of, 528
Corythomantis (amphibian: an anuran),
Cott, 341, 544, 546 [pupil of, 223

Cottidse (teleosts: sculpin and muddler fam-
ily), pleated conjunaiva in, 454
Cottus (teleost: a cottid), dermal color

changes in, 481
Cotylosauria (earliest reptiles)
closeness of chelonians to, 608
color vision in, 520
sclera in, 274

taxonomic position of, 135, 608
visual cellsof, 612, 621,637, 691
cougar (American lion), eye and nasad

asymmetry thereof, 173, 300, 678
cow: Bos, q.v.

Crampton, 524; muscle of, 279*-281, 280,
Crenilabrus (teleost) [441, 646

dermal color changes in, 481-482
development of sclera in, 579
Creodonta (extinct mammals), 675-676
crepuscular: active in twilight — specifically,

evening twilight (c/. auroral)
Criinas (amphibians: bufonid sub-family),

vertical pupil in, 223
Crocidura (mammal: a shrew), visual cells

in, 685
Crocodilia (alligators, caymans, crocodiles,
gavials)
accommodation and refraction in, 251,

272-274, 279, 436, 614
adnexa of, 162,421-422, 436
area centralis in, 184-185, 187, 616
coloration of eye and body in, 613
color vision in, 496, 519
comparison with sirenians and whales, 422
conus papillaris in, 615, 653, 657
departure from standard reptilian pattern,
dermal color changes in, 542-543 [622

eye movements in, 305

eyeshine and tapetum lucidum in, 231,

238, 240, 616, 654
fibrous tunic in, 270, 274, 613
habits of, 145, 150, 162, 184-185, 200,
lens in, 614, 620 [274,436,543

ocular size and shape in, 613
pupil in, 145, 162, 220, 224, 238, 496

speed of, 150,501, 614
resemblance to monotremes, 669
retina in, 162, 615-616

photomechanical changes of, 150, 162,
taxonomic position of, 135, 138 [238

uveal tract in, 613-614, 623, 654
visual acuity in, 184-185, 207
visual cells in, 200, 615-616, 621, 661

oil-droplets claimed for, 616
visual fields of, 293-294, 443
Crocodilus (reptile: a crocodilian), adnexa

in, 422
Crossopterygii, 136* (see also Latimeria) ,
as ancestors of Amphibia, 135,
588-589
Crotalidae (reptiles: pit-viper family; see also
Agkistrodon, Crotalus, Trimer-
habits of, 201 [esurus)

pupil in, 165,221,225
retina in, 165

visual cells in, 166, 639-640
Crotalus (reptile: rattlesnake)
dermal color changes in, 542
spectacle in, 450

development of, 454-455
Crotaphytus (reptile: an iguanid lizard),
Crozier, 520 [visual cells of, 62, 626

crumen: a cheek gland of ruminants; 546
Cryptobranchidae (amphibians: a urodele

family; see Cryptobranchus, Megat-
chararteristics of, 600 [obatrachus

sclera in, 601
Cryptobranchus (amphibian: hellbender)
habits of, 407

thick scleral cartilage of, 415, 602
visual field of, 291
Cuniculus (mammal: spotted cavy)
pupil of, 221

tapetum lucidum (unique for rodents)
and eyeshine of, 230, 233, 241
Cyclopean eye, physiological, 324*
cycloplegic, 447*

cyclostomes: Cyclostomata (lowest vertebrate
class, comprising lampreys and
hags, qq.y.}, 135*-136, 555-562,
sub-index p. 555.
Cyclothone (deep-sea teleost), photophores

of, 402
Cygnus (bird: a swan), eye of, 643
Cynictis (mammal: a viverrid carnivore)
diurnality of, 686

INDEX AND GLOSSARY

737

horizontal pupil of, 221, 227, 299

tapetum lucidum (lacking) in, 241
Cynomys (mammal: a sciurid rodent;

area centralis of, 187 [prairie-dog)

habits of, 205, 312

mobility of eye in, 312

optic disc of, 180

pupil of, 221

retina of, 176, 513, 659, 684

visual acuity of, 312

visual cells of, 685

yellow lens of, 143, 199
Cynopterus (mammal: a fruit-bat), retinal

tapetum lucidum of, 684
Cyprinidct (teleosts: minnow family)

chorioid gland in, 581

conjugate cones in, 586

cornea in, 579

development of sclera in, 578-579

guanin tapetum lucidum in, 236, 240, 585,
692 (entry for p. 236)
Cyprinodontidffi (teleosts: killifish family),
taxonomic position of, 576-577, 587
Cyprinus (teleost: carp)

color vision of, 478, 489-490

form-discrimination of, 489-490

lens and ultra-violet light, 375
Czermak, 236

dace (see Chrosomus, Semotilus)
dachshund, visual hunting by, 345
Damomanta (elasmobranch: a ray), pupil

of, 220, 222
Daltonism: hereditary dichromatic color

blindness; see color blindness and
p. 692 (entry for p. 99)
dark-adaptation 73*, 76-80
darters (teleosts), yellow cornea in, 202
Darwin, 438, 466
Dasyatis (elasmobranch: a ray), pupillary

operculum of, 222
Dasypeltis (reptile: egg-eating snake), visual

cells of, 166, 638
Dasypus (mammal: armadillo)

cornified and vascular cornea in, 665, 678

eye of, 680

eyeshine of, 241

lid closure in, 427

pupil of, 221

retina of, 216, 685

taxonomic position of, 139, 676
Dasyurus (mammal: marsupial 'cat')

ciliary muscle of, 673-674

pupil of, 221, 227

retinal vessels of, 672-673

tapetum lucidum of, 241, 672
Davenport, 524

Davis, 507

dazzlement (see glare and dazzle)

decussation, 47, 52*, 335

partial, value of, 320-323, 328-331
total

and impermanence of correspondence,

meaninglessness of, 5>2, 322 [330

w partial, 52, 319, 323-331, 532

simulation of, 321-322
deep-sea fishes, eyes, habits, and habitats
of, 391-405
accommodation (impossible) in, 257, 262

substitutes for, 254, 257
argentea (lacking) in, 235
'bifocal' optics in, 257
binocularity in, 290, 320, 329, 331, 401-

403, 413
eye movements (lacking) in, 329
fovea in, 190, 402
iris (lacking) in, 160-161
large eyes in, 209-210, 395
larvae of, 403-407, 404

prsescopic, 40 1 , 405
lens in, 257, 262, 399-402, 400-401
loss of deep-sea habit by, 388, 399, 586
luminescence of, 396-398, 402-403
multiple optic papillae in, 367
optic chiasma of, 329
retina in, 399, 585-586

accessory, 257, 400

summation of, 400, 568
sclera in, 415, 565
size of, 395
tapetum lucidum in, 398

fibrosum, guanin in, 239

retinal, 238, 585
tubular eyes in, 212-213, 262, 264, 400-

development of, 400-40 1 [ 403

vestigial eyes in, 397-398
visual cells of, 399, 568

concentration of, 396, 399-400

length of, as substitute for accommo-
deep-sea habitats [dation, 254, 399

characterization of, 393-398
classification of, 392-393
deeps (of ocean), 393*
deer: Cervida, q.v.
deer-fly, speed of, 351-352
degenerate eyes

eye muscles and, 300

produced by darkness, 390

recrudescence of, 390

speaacle in, 450, 453, 458-459

taxonomically:

cyclostomes, 210, 387, 391, 562

teleosts, 210, 300, 384, 387-391

dipnoans, 589-590

amphibians, 210, 300, 407, 600, 605-606

738

INDEX AND GLOSSARY

degenerate eyes — cont'd

lizards, 210, 625

snakes, 210, 627, 687

bird, 650

mammals, 209, 671, 677, 687
degeneration of retina, 228
delamination: a separation into layers
Delphinidae (mammals: dolphins, porpoises),

412
Deltdtheridium (extinct mammal), 675
Dendrobates (amphibian: an anuran), poss-
ibility of yellow filters in, 599
Dendrolagus (mammal: a tree-kangaroo),

size of eye and lens in, 674
Denisonia (reptile: an elapid snake), visual

fields of, 294
depth, perception of, 315*

binocular, 314-319

monocular, 313-314

in animals, 323, 341-342

in paintings, 194
depth of focus, 68, 254
dermal color changes (see color changes)
Dermoptera (order of mammals: flying-
lemurs), taxonomic position of,
139, 676
Descemet, corneal layers of, 8, 10, 11*-12

absence of, 623

development of, 116

origin of, 451-452

taxonomically:

lampreys, 557

elasmobranchs, 566

sturgeons, 570

holosteans, 574

teleosts, 580-581

dipnoans, 590

anurans, 595-596

chelonians, 609

Sphenodon, 617

lizards, 623

monotremes, 667-668

marsupials, 672, 674

placentals, 678-680
man, 8, 10, 11-12
deserticolous : desert-inhabiting
Desmognathus (amphibian: dusky salaman-
der), retinal summation in, 603
deuteranopia, 99*
development (embryology) of:

amphibian vitreous, 188

annular ligament, 580

annular pad, 276-277

anterior segment, I 15-116

Apteryx eye, 650

caecilian eye and adnexa, 606

conus papillaris of snakes, 631

deep-sea fishes, 400-401, 404-405, 404

Didelphis eye, 663, 672

eel, 405-407

eye muscles in sharks, 564, 567

eyeball wall, 114-115, 593-594, 601-602,

Gemminger's ossicle, 643 [629

glands, 115, 117,445, 593

iris muscles of birds, 647

iris muscles of snakes, 630

lamprey eye, 117-118, 126-127, 131, 406-

lens, 105-113, 106, 110-112 [407

lids, 118, 452, 593, 601,644

mammalian eye, 104-117

median eyes, 126, 338

nictitating membrane, 118

optic cup, 104-108, 105-106

pecten, 118, 648

retina, 106-109, 107, 582, 602

retinal vessels, 112-113, 684
murid rodents, 684

spectacle, 454-455

stalked eye, 404

tubular eye, 401

vitreal vessels in snakes, 631

vitreous, 113-118, 114,610-611
Devonian ocean, salinity of, 370
DeVoss, 506
Dialommus (teleost: four-eyed blenny), eye

of, 433-434
DibamidcB (reptiles: a fossorial lizard

eyes of, 625 [family)

spectacle in, 450
Didelphis (mammal: opossum)

achromatic vision of, 518

area centralis of, 185

ciliary muscle of, 674

cornea of, 671

disappearance of choriocapillaris in, 672

eye of, 173

development of, 663

eyeshineof, 231, 238, 241

fundus of, 233

method of eye closure in, 427

optic chiasma of, 319

retina in 239, 672

vessels of, 201, 654, 672

tapetum lucidum of, 143, 233, 245, 238-
239, 241, 654, 672, 684

visual acuity of, 207
Diemenia (reptile: an elapid snake), visual

fields of, 294
diencephalon, 105*; photosensitivity of, 79,
digitonin, 75 [127-128

dimorphism: the occurrence of two struaural

types within a single species
Dinichthys (extinct fish), scleral ossicles of,
dinosaurs, 138 [380

as ancestors of birds, 138, 622

probable habits of, 164, 203

INDEX AND GLOSSARY

739

taxonomic position of, 135
visual cells of, 621
Diomedea (bird: albatross)
eye and scleral ossicles of, 270
feeding method of, 439
diopter, 34-35*, 194, 447
dioptric media : cornea + aqueous + lens +
absorption in, 194, 196, 199 [vitreous
dispersion by, 193-194
maximal transparency of, 609
passage of light rays through, 29-30
dioptrics, 417, 428-448, 455
diphyletic: said of an animal group once
supposed to have had a single com-
mon ancestor, but now known to
comprise two real groups, each
with a separate common ancestor
Diplasiocoela (amphibians: an anuran sub-
order), taxonomic position of, 593
diplopia, 318*, 324
of median eyes, 340
monocular, 330

physiological, 317-318, 330, 361
in strabismus, 329-330
Dipneusti: Dipnoi, q.v.
Dipnoi (dipnoans; lungfishes)
accommodation in, 263
chorioid in, 590
comparison with lampreys, 590
dermal color changes in, 525, 537
fibrous tunic in, 590
habits of, 150, 200, 223, 263
iris in, 590
lens in, 590
optic nerve in, 591

pupil in, 150, 160, 220, 222-223, 590
relationships of, 135-136, 588-589, 593
retina anci visual cells of, 150, 200, 216-

217, 590-591,600
size of cells in, 217, 591
spectacle in, 450, 590
vitreal vessels in, 590
dipper (bird: water-ouzel)
cloudy nictitans of, 424
habits of, 439
lacrimal gland in, 425
Dipsadomorphus (reptile: a colubrid snake),

visual cells of, 638
direction, local signs of (see local signs)
Discoglossus (amphibian: an anuran), scleral
Disney, 360 [cartilage of, 595

Dispholidus (reptile: a colubrid snake),

visual fields of, 294
Dissomma (deep-sea teleost), development

of tubular eye in, 400-401
distance, perception of, 315*
binocular, 314-315,317
factors in, 247-248, 313-314, 344

monocular, 313-314

in animals, 323, 341-342

through 'growth' of image, 344

value of vision in, 288

'visual trident' and, 307-310
diurnality (see also habits)

adaptations for, 169-205, 208, 609, 617,
620, 622, 624-625, 630, 636-640,
642, 675, 684-689

and color vision, 464, 504-505, 518-521

ocular proportioning in, 1 73, 609

pupil and, 217-228, 627

retinal lamination in, 177

retinal metabolism in, 652, 658

tertiary, 627
diving, by:

birds, 226, 438-442, 647

fiishes, 415-416

humans, 349

seals, 444

whales, 415-416
Dodge's experiment, 348*
dog (a canid carnivore)

accommodation of, 156

color vision in, 505-507

convergence in, 312, 328

eye of, 173

movements of, 311

optic axes of, 297

optic chiasma of, 319

perception of movement by, 350, 362

pigment epithelium of, 56, 238, 684

pupil responses of, 156, 501

retractor bulbi muscle of, 420

stroboscopic vision in, 362

surgical interchange of eye muscles in, 311

tapetum lucidum of, 234, 684

visual field of, 297-298

visual hunting by, 345
dogfish

true: any of several small sharks

'freshwater-': Amia, q.v.
Dolichopteryx (deep-sea teleost), vertical

aim of eyes in, 401
Dolichotis (mammal: Patagonian cavy),
diurnality of, 686, 692 (entry
for p. 201)
dolphin: a small whale, q.v.
dominant ('master') eye: the eye which one
prefers to use for one-eyed tasks,
such as sighting a rifle or looking
through a telescope or microscope

role of, in binocular vision, 90, 324
Donders, laws of, 302
dormice (mammals: rodents; see Eliomys,

chorioid in, 654 [Glis, Muscardinus)

pupils of, 162

retinal vessels of, 654

740

INDEX AND GLOSSARY

dorsad: toward the back (not posterior end)
of an animal; thus, for a four-
footed animal, upward
douroucouli: Aotus, q.v.
Dove's experiment, 315*
DromcEus (bird: emu), pecten in, 649
dromedary (one-humped 'camel'), eye of,

173
Dryophiops (close relative of Dryophis,q.v.)

adaptations for binocular vision in, 299,

fovea of, 186-187, 307 [307

pupil of, 692 (entry for p. 221)
Dryophis (reptile: East Indian long-nosed

accommodation in, 283, 299 [tree-snake)

binocular vision in, 186, 293-294, 307

cheek groove of, 185-186, 299

dermal color change in, 542

eye-movements in, 307

fovea of, 185-188, 186, 307

habits of, 178

head of, 186

independence of motion of prey, 344

possible color vision of, 520

probable color of lens in, 199

pupil of, 185-186, 221, 293

visual acuity of, 178, 637-638

visual cells of, 178, 637-638

visual fields of, 292-294
duck-bill: Ornithorhynchus, q.v.
ducks

dabbling, ciliary muscles of, 441

diving

ciliary muscles of, 441
cornea of, 441
iris sphincter in, 440
nictitans-lens in, 440

feeding habits of, 439

torrent-, 439

visual fields of, 295
Dufay, 503
Dugong (mammal: a sirenian)

eye and habits of, 408-410, 409

refraction of, 273
Dunlap, 692 (entry for p. 99)
Duplicity Theory, 64*, 65*-73, 657

attacks upon, 215

color-vision tenet of, 463-464

photomechanical changes and, 149

physiological evidence for, 70, 71-73, 149,
500

visual-cell transmutation and, 163-168,
464-465, 497
dura mater (see meninges)

eagle-rays: Myliobatidae, q.v.
eagles

area and foveae of, 187, 307-308

eye shape in, 642-643
feeding methods in, 439
oculorotatory muscles of, 642
pecten in, 643, 655-656
retina, area of, 656
scleral ossicles of, 270, 644
visual capacities of, 655, 662
earthworm, photoreceptors of, 3
echidnas (monotremes; see Tachyglossus,
behavior of, 185 [Zaglossus)

circumlental space in, 284
eyes of, 664-671,667
lenses of, 284
lids of, 425, 427
visual cells of, 670-671, 688
ectoderm: outermost of the three germinal
cell-layers of an embryo (see endo-
derm, mesoderm)
ectopic: out of the usual place
edentates, 676*
Edridge-Green, 499

eels (teleosts; see also Angullla, Gymnotidae,
Simenchelys)
campanula (lacking) in, 583
chorioid gland and pseudobranch (lack-
ing) in, 581
cornea and spectacle in, 450, 454
falciform process (lacking) in, 582
habits of, 372
life cycle of, 405-407
pupil in, 150, 220

retinal vessels of, 51, 202, 204, 582-583
Egger's line, 10, 19*
Egyptians, reverence of cat by, 234
eikonogenesis, 3*

Elapidse (reptiles: cobra-type snake family)
fossorial, spectacles of, 450
habits of, 201
pupil in, 221, 225
visual cells in, 201, 637-638
yellow lens in, 201
elasmobranchs: Elasmobranchii (lowest class
of true fishes, comprising sharks,
rays etc., and chimjeras); 563-569;
see also Batoidei, sharks, Holo-
cephali; 692 (entries for pp. 561,
568)
electric organ, evolved from eye muscles,
electric ray: Torpedo, q.v. [293

eleCTroretinogram, 490* (see retina, photo-
electric phenomena of)
elephant-fishes: MormyridcE, q.v.
elephant-seal: Macrorhinus, q.v.
elephants

cones of, 688
eye size in, 145
eye-movements in, 311
habits of, 145

INDEX AND GLOSSARY

interpupillary distance of, 327

lashes (lacking) in, 426

lid movements of, 425

optic axes in, 297

tapetum lucidum of, 145, 233, 241

taxonomic position of, 139, 676

thick sclera in, 415
Eliomys (mammal: a dormouse), retinal

circulation in, 201
elk, taxonomic position of, 139
ellipsoidality (ellipticity) of eyeball

and barrel distortion, 354

and lid-opening, 428

and streamlining, 380-381

taxonomically:

elasmobranchs, 565, 569

sturgeons, 569

holosteans, 574

teleosts, 578

birds, 643

mammals, 677
seals, 445
sirenians, 409
toothed whales, 414
Ellohius (mammal: a mole-rat), eyes of, 677
Elritz, Ellritz: Phoxinus, q.v.
ElopidcB (teleosts: ten-pounder family)

guanin in retina in, 585

visual-cell bundles in, 588
Elops (teleost: ten-pounder)

adipose lids of, 383

leptocephalus stage of, 406
embryology: development, q.v.
embryonic fissure (see optic cup)
emmetropia, 27, 35-36*, 249*, 252-253,
emu: Dromceus, q.v. [288, 407

Emyda (reptile: a terrapin), lid window in,
Emys (reptile: a terrapin) [450,457-458

accommodation in, 437

anterior segment of, 277

behavior of, 494

circulatory pattern of eye in, 611

scleral ossicles of, 274
Encheliophis (teleost: pearl-fish)

dorsal aim of eyes in, 160, 391

habits of, 391

pinhole pupil of, 160, 220, 222, 228, 257,

tendinous sclera of, 578 [273, 391

endoderm: innermost of the three germinal
cell-layers of an embryo (see eao-
derm, mesoderm)
English sparrow: Passer, q.v.
Engraulis (teleost: an anchovy), eye and

tertiary speaacle of, 454, 460
entoparasite : an internal parasite
Entosphenus (cyclostome: a lamprey)

chorioid of, 558

size of eye in, 556

visual cells of, 560-561
Eosuchia (extinct reptiles)

eyes of, 622

taxonomic position of, 135

visual cells of, 621, 637, 691
ependyma, 127*, 127

in Amphioxus, 128

in lampreys, 128

in optic nerve, 559-560, 569, 591, 632

origin of visual cells from, 126, 127-129

vacuolated, 573
EpicTdtes (reptile: a boa)

canal of Schlemm in, 629-630

ciliary body of, 629

sclera of, 627

zonule fibers of, 631
Epigonus (deep-sea teleost), enlarged eyes

of, 395
Epinephelus (teleost: grouper), dermal color

changes of, 528
epithelium: a sheet or pavement of cells of
either ectodermal or endodermal
origin (cf. mesothelium)
Epomophorus (mammal: a fruit-bat), retinal

tapetum lucidum of, 684
Eptatretus (cyclostome: a hag), eye of, 562
Eremias (reptile: a lacertid lizard), lid win-
Erhard, 501 [dow of, 450

Erickson, 93
Erinaceus (mammal: hedgehog)

color vision in, 517

Meibomian glands of, 665

retina of, 216, 685

taxonomic position of, 676
erythrophores, 526*
Eryx (reptile: sand boa)

canal of Schlemm (lacking) in, 629

fibrous tunic of, 628

lens of, 630
Esox (teleost: pike)

binocular field of, 292

cornea of, 579

Descemet layers of, 580

yellow coloration of, 191, 200, 202

dermal pigments, effect of light on devel-

habits of, 200 [opment of, 534

optic nerve and disc of, 179

retina of, 200, 433

horizontal cells of, 585

scleral cartilage and ossicles of, 380
essence d'orient, 235*
Etmopterus (elasmobranch: luminous shark)

depth of swimming in, 392, 416

eye size in, 416, 563

lens of, 563

luminous organ of, 402

pupil of, 222, 398

retina and visual cells of, 399-400, 568

742

INDEX AND GLOSSARY

Etmopterus — -cont'd

tapetum lucidum of, 398
thin sclera of, 416, 565
Etrumeus (teleost: near anchovies) spectacle

of, 460
Eublepharidje (reptiles: lidded gecko family)
habits of, 201
lids of, 458, 623
pupils of, 220
taxonomic status of, 623
Eublepharus (reptile: a eublepharid lizard),

'lashes' of, 424
Eucalia (teleost: a stickleback), color vision

of, 483
Euchirotidae (reptiles: a fossorial lizard
eyes of, 625 [family)

spectacles of, 450
Eudontomyzon (cyclostome: a lamprey),

size of eye in, 556
Eudyptes (bird: rockhopper penguin), sea-
sonal change of iris color in, 550
Eumetopias (mammal: a seal), ocular pro-
portions in, 445-446
Euphagus (bird), nuptial changes of iris

color in, 550
Eurycea (amphibian: a urodele), retinal

summation in, 603
Euscorpius (arthropod: a scorpion), ocellus

of, 3
Eustomias (deep-sea teleost), stalk-eyed

larva of, 405
evagination: an out-bulging or out-pocketing
Evermanella (deep-sea teleost)

guanin retinal tapetum lucidum of, 237-

238, 240
normal and tubular eyes in different
species of, 400
Eviota (teleost), internal coloration of, 528
evolution, of:

accommodation, 272-273 (Table VIII)
amphibians, 593, 600-601, 604-605
area centralis and fovea, 181-184
binocular vision, 326-331
birds, 641

as read in scleral ossicles, 274
cave habit, 387-390
color vision, 463-465, 518-521, 519,

688-689
conjunctiva, cornea, and spectacles,

449-461, 451
control of visual-cell illumination, 150

(Table II)
deep-sea fishes, 391-403
eye, 104, 119-133, Part III

degenerate, 209-210, 384, 387-390,
diurnal, 175, 608 [397-398

median, 338-340
nocturnal, 210-212, 608, 614, 621

terrestrial, 417-420, 592-593, 607
tubular, 212, 400-403
in water, 369-371, 462

flatfishes, 385

intra-ocular color-filters, 199-205, 200-201,

lungfishes, 588-589 [(Table IV)

mammals, 663-664, 675-676, 686-689

nocturnality, 208-209

pupil, 220-221 (Table VI)

retinal nutrition, 648-659

seal eye, 448

snakes and their eyes, 458-459, 543, 632-

tapetum lucidum, 243-245 [640

teleosts, 576-578

vertebrates, 134-139, 135

vertical slit pupil, 428

visual cells, 62-63, 163-168, 691 (Plate I)
Exner, 366

extra-ocular muscles (see muscles)
eye, simulation of, 544, 548
eye-masks, 545-547
eye-mindedness, 283
eye-movements

are«, fove», and, 288, 300-312

avoidance of, 312

binocularity and, 291, 323-331, 340

classification of, 300

downward, 387

gyroscopic, 303, 348-349

labyrinth and, 301

local signs of direction and, 330

passive, and diplopia, 318

pursuit, 348, 352

reading and, 348-349

reconjugation of, after surgery, 311-312,
328-329

retractive, 303, 305, 386, 419-423, 427,
429-43 I
swallowing aided by, 419, 594, 601

saccadic, 348

suppression of vision in, 348-349

simulation of blinking by, 387

space-perception and, 300-312, 348-349

spectacle and, 449, 452-454

wheel-, 303, 564-565

taxonomically:

lampreys, 259

fishes, 303-305, 429, 564-565

amphibians, 305

reptiles, 305-306

birds, 307-310

mammals, 310-312

man, 38, 300-302, 311, 314-318, 328-
whales, 412 [331,347-349

eye-spots, 544-545
eyelessness, absolute, 397-398
eyeshine, 229*

in birds, 646

INDEX AND GLOSSARY

color of, 23 1

distribution of, 240-241 (Table VII)
eyestrain, 269

falciform process, 118, 261-262*, 567, 575,

577, 582-583*, 653 (see also
falcon (see hawks) [648-659)

falconry, 169
Farancid (reptile: a rainbow snake)

accommodation in, 438

chorioid of, 629

pupil of, 221, 225

scleral pigment in, 628

spertacle of, 450

visual cells of, 165, 640
far point, 252*, 252
far-sightedness: hypermetropia, q.v.
'fatigue' (for colors), 93
Fechner, law of, 534-535*
FelidcB (mammals: cat family; see cats)
Felis (mammal: most cats ), anterior segment
ferret: Putorius, q.v. [of, 683

Ferry and Porter, law of, 72
fibrous tunic: cornea -i- sclera, qqv.
Fick, 98

Fierasfer: Encheliophis, q.v.
fighting-fish, Siamese: Betta, q.v.
filefish: Monacanthus, q.v.
Fincham, 33
finches, eye size in, 641
Finlay, 503
fishes, 134-137, 555-591, sub-indices on pp.

555, 563, 569, 573, 589
fishing (angling) and color vision, 472
Fitzroya (teleost), evidence for chromato-
phore-controlling hormone secreted
by eye of, 530
fixation: aiming a particular spot of the retina
at a particular point in space

binocular, 311,317-318

eye-movements and, 300-312

universal macularity and absence of, 312
flamingo, area and fovea of, 187
flatfishes (see also Bothidje, Pleuronertida,

binocular field of, 292-293 [Soleids)

color vision in, 482, 527-528

dermal color changes of, 482, 526, 529-

evolution of, 385 [530, 533-534

eye-movements of, 303

habits of, 374, 386

pupils of, 220
movement of, 150
opercula of, 158, 160, 220, 222, 386

retinal pigment migration in, 150

turreted eyes in, 386
temporary lids of, 432

visual cells of, 150, 586

Flamming, 526

flicker (of lights); see fusion, critical

frequency of
flicker (a woodpecker) : Colaptes, q.v.
flounders: flatfishes (in part), q.v.
flower colors and color vision, 503-504
fluviatile: inhabiting running water, as rivers
flyingfishes

freshwater: Pantodon, q.v.
time spent out of water by, 43 1
ventral binocular field of, 293
flying-frog: Polypedates, q.v.
flying-lemurs: Dermoptera, q.v.
flying-snake: Chrysopelea, q.v.
Fontana, spaces of, 441, 570, 679-680*
form discrimination, by carp, 489-490
fossorial vertebrates (see habits, fossorial)
'four-eyed' fishes: Anableps, Dialommus,
fovea, 181* [<iq-'>'-

aphakic space and, 299, 305
'bifocal', 442

chromatic aberration in, 195
clivus of, 188*
cone-density in, 625, 661
as corresponding point, 317-318, 322
depth of, 184, 187 (Table III)
distribution of, 184-186, 187 (Table III),
188-190, 303-312, 387, 588, 611,
620-621, 625, 689
effect of domestication on, 190
externa, 182*

eye-movements and, 288, 291, 300-312
fishes, 303-305
reptiles, 305-307
birds, 307-310, 442
mammals, 310-311
length of visual cells in, 195, 692 (entry

for p. 195)
muscle cells associated with, 281
oil-droplet colors in, 193
optical function of, 182, 183, 184
pure-rod, 189-190, 402, 621
relation to area centralis and macula lutea,
stimulation of, 71-73 [ 181-184

substitute (see macula, substitute)
taxonomically:
teleosts, 184-185, 188, 292, 304 (list),

deep-sea, 190, 402 [305

Amyda, 184, 186, 190
Sphenodon, 188-190, 189, 617, 620-621
lizards, 173 (chameleon), 188, 625, 632
snakes, 185-186, 188
birds, 182-183, 188-189, 190, 193, 308-
309, 661-662, 692 (entry for p.
195)
primates, 7, 182, 188, 190, 661-662,
685, 689
foveolae optica, 105*, 119, 122-123

744

INDEX AND GLOSSARY

fowl, domestic: Callus, q.v.

Fox, 534

foxes: Vulpes et al

flying-: Megachiroptera, q.v.

optic axes of, 297

pupils of, 162, 227

tapetum lucidum in, 232
Franz, 131-132, 139, 284, 286, 372, 406,

429, 655, 661, 664, 666, 677
freezing posture, 309, 344-345
Freytag, 481
Friedrich, 492-493
Frima, 515, 521

von Frisch, 474, 479-483, 531-532
frogmouth: Podargus, q.v.
frogs: Anura (in part), q.v.; see also Rana,
frontality, 290* [Ranidae

binocularity and, 3 1 1

ocular mobility and, 309

partial decussation and, 320
Froriep, 119, 121-122
fruit-bats: Megachiroptera, q.v.
fry: young fish
Fuchs, 542

Fiirst, fiber of, 55, 58
fuliguline ducks, 441
Fundulus (teleost: killifish)

dermal color changes of, 481, 525-526,
532, 534

double (?) cone of, 59, 587

dual ares centrales in, 188
fundus, 47*

fuscin: the melanin-like pigment of the ret-
inal pigment epithelium, 236-237,
fusion [478, 585, 659

binocular

basis of, 320-326, 331-338
cerebral center of, 90-91, 321, 335
kinds of, 333-334
mosaic theory of, 324, 333
prerequisites for, 315-319

of colors, 83-84, 90-91, 335, 355, 364-365

critical frequency of, 70, 72*, 350-365, 520

psychic, 91, 321, 322*. 323, 334-335,
337-338

G

Gadids (teleosts: cod family)

accommodation (lacking) in, 583

campanula (lacking) in, 586

falciform process in, 582

origin of, 399, 586, 636

scleral ossicles (lacking) in, 586

visual-cell mosaic in, 588
Gadus (teleost: cod)

annular ligament of, 581

falciform process of, 582

visual cells in, 586

Gaffron, 363-364

Galago (mammal: a lemuroid)

color blindness of, 520

frontality of, 327, 331

pupil of, 228

tubulareyeof, 213, 677-678
Galeopithecus (mammal: a flying-lemur),

139, 676
Galeopterus (mammal: a flying-lemur),

139, 676
GaleorhinidcB (elasmobranchs: requin shark
family), 692 (entry for p. 386)

lid complex of, 382, 386, 429, 563
GallinacesB (birds: fowls etc.; see also

G alius), pecten in, 655
gallinules, head movements of, 342
G alius (bird: domestic fowl)

accommodation of, 281

binocular field of, 298, 307

color vision of, 497-502

distance-judgement of, 327

flight muscles of, 164

fovea (lacking) in, 190

head movements of, 342

oil-droplets in

pigments of, 192, 198
red field of, 307, 502

pecten of, 649

retina of, 659-660

visual acuity of, 207
Gambusia (teleost: mosquito-fish)

protective coloration of, experiments with,

dermal color changes of, 524, 534 [524
gannet, Morus, q.v.
'ganoid' fishes, 137*
Ganson, 506

Garrulus (bird), pecten of, 655
gars, 'gar-pikes': Lepisosteus, q.v.
garter snake: Thamnophis, q.v.
Gasserian ganglion, 1 72
Gasteropelecus (teleost: hatchet-fish), flight

of, 431
Gasterosteus (teleost: a stickleback)

color-associations and brain surgery in, 522

color vision in, 483, 487-489, 522

lens and ultra-violet light, 375, 488-489
Gates, 505
Gazelle (mammal: an antelope), corpora

nigra of, 219
geckoes (lizards: Gekkonidee -(- Eublepharidas

accommodation in, 254 [-1- Uroplatus)

ciliary muscle in, 624

classification of, 623

color vision in, 520

contrasted with snakes, 634

conus papillaris in, 625, 653, 658

dermal color changes in, 540-541

Descemet's layers (lacking) in, 623

INDEX AND GLOSSARY

745

diurnal, 201, 203, 520, 627 (list)
visual cells of, 627
yellow lenses in, 191, 199, 201, 203
fovea in, 621, 625
fusion frequency for, 72, 520
habits of, 145, 168, 201, 203, 219, 458,
lens in, 620 [627, 658

lidded: Eublepharidae, q.v.
pupils of, 166, 168, 203, 220, 223-224,
spectacles of, 450, 458 [272-273, 627

visual capacities of, 206, 465, 497
visual cells of, 62-63, 168, 200, 203, 216,
254, 520, 626-627, 653
mosaic of, 638
Gekkonid2e (reptiles: spertacled gecko family)
Gemminger, ossicle of, 643-644
Gennari, stripe of, 334-338, 335
Geomyda (reptile: a terrapin), binocular

field of, 294
Geotria (cyclostome: a lamprey)
habitat of, 555
habits of, 199-200
relationships of, 555, 562
size of eye in, 556
visual cells of, 561-562
Gerould, 524
giant salamander, Japanese: Megalo-

batrachus, q.v.
Gigantura (deep-sea teleost), tubular, for-
ward-aimed eyes of, 402-403
Gila monster: Heloderma, q.v.
Gillett, 611-612
Gillichthys (teleost), dermal color changes

in, 534
Gingylostoma (elasmobranch: gata or

nurse shark), pupil of, 222
giraffe, optic axes of, 297
GirelLi (teleost: sea bream)
dermal color changes of, 534
fovea of, 187, 304
glands (associated with eye)

development of, 115, 117, 445, 593
endocrine, 581

Harderian, Harder's; taxonomically:
amphibians, 419, 430, 594, 601,
chelonians, 423 [605-606

crocodilians, 422
Sphenodon, 420
lizards, 423
snakes, 424, 455-456
birds, 425
monotremes, 665
marsupials, 671
shrews, 426
rodents, 426
sirenians, 408
whales, 412
seals, 445

infra-orbital: crumen, q.v.
lacrimal, TAXONOMICALLY:
amphibians, 419, 430, 601
chelonians, 423
crocodilians, 422
Sphenodon, 617
lizards, 423, 617
birds, 425
monotremes, 665
marsupials, 671
placentals in general, 426
seals, 445
sirenians, 408
whales, 412
man, 39, 41
of Meibom, 39, 40*, I 15, 412, 426, 445,
oil, sebaceous), of lids [665

crocodilians, 422
sirenians, 408
whales, 412
of Zeis, 39, 40*
glare and dazzle, 195, 245, 429, 433, 437
glass membrane: lamina vitrea; 42*-43
in lizards, 624

in ostrich (serving as tapetum?), 230
in Sphenodon, 617
in teleost iris, 584
Glaucomys (mammal: flying-squirrel; see
glioma, 49* [squirrels)

Glii (mammal: a dormouse)
pupil of, 221, 227
retinal circulation in, 201
glucose, 583, 653

glycogen: animal starch; 574, 581
gnathostome fishes: non-cyclostomes; eye-
muscle plan in, 565
goat

interpupillary distance of, 327
visual field of, 298
goatsuckers (bird family Caprimulgidje)
as ancestors of owls, 309, 656
crepuscularity of, 208
eye-closing habit in, 546-547
eyeshine in, 240, 646
feeding method of, 169
pecten in, 656
gobies (teleost family Gobiidas)
amphibious habits in, 432
blind, eyes of, 387-388
limicolous, 210
spectacles in, 450
Gobius (teleost: a goby), color vision of , 483
golden moles

marsupial: Notoryctes, q.v.
placental: Chrysochloris, q.v.
goldfish: Carassius, q.v.
Goldsmith, 483
Golgi, 568

746

INDEX AND GLOSSARY

Gonatodes (reptile: a spectacled gecko)

pupil in, 203, 220, 627

visual cells of, 627
Gonorhynchus (teleost), spectacle of, 460
goose

pecten in, 656

terrestrial, Australian: Cereopsis, q.v.
gorilla

diurnality of, 228

frontality of, 327
goshawk: Accipiter, q.v.
Graber, 472-473, 476
grackles, change of eye color in, 550
Granit, 78, 490
Graptemys (reptile: a terrapin), white iris

in, 550
grass snake, European: N. natrix, q.v.
gray snapper: Lutianus, q.v.
grebes, underwater swimming of, 439
Greeff, 586
Gregg, 507

grenadiers: Coryphcenoididce, q.v.
Gresser, 665
Grether, 515-516
greyhound, visual hunting by, 345
Grinnell, 341
Grossman, 291

groupers: Epinephelus {q.v.), et al
Grynfeltt, 589; sphincter of, 160*, 584
guanin, 235*

in argentea, 235-236, 270

in iridocytes, 526, 543

in tapeta lucida, 235-243, 570, 585, 692
guano, 235* [(entry for p. 236)

guanophores: iridocytes, q.v.
Gudden (see Newton-Miiller-Gudden)
guinea-pig

color vision in, 512

intelligence (lacking) of, 467

pupil of, 157

retina of, 157, 216, 685

visual field of, 298
gulls

area and fovea of, 187

feeding method of, 439
Gunn, 664, 669
guppy: Lebistes, q.v.
gurnard: Trigla, q.v.

'flying', flightlessness of, 431
Gymnophiona: Ccecilia, q.v.
GymnotidcE (teleosts: an eel family),

tendinous sclera in, 578
gyroscope-like action of eyeball, 303, 310,
348-349

habits of vertebrates

aquatic (see aquatic activity)

amphibious (see amphibious aaivity)
basking, 200, 218-219, 222, 224, 571
cavernicolous (see cave-dwelling verte-
brates)
circulatory structures of eye and, 648-659
deep-sea (see deep-sea fishes)
of earliest vertebrates, 163-164
evolutionary changes of, 165-168
eye-mindedness, 283

feeding, and as to light, 169-171, 208-209
fossorial, 200-201, 209-210, 605-606

and blindness, 390, 458, 625

and origin of snakes, 634

and spectacles, 457-459
freezing, 309, 344-345, 546
intensity of light and, 143-145, 149-150,
154-163, 197-210, 215-246, 545,
684, 692 (entry for p. 201)
intra-ocular color-filters and, 200-201
locomotor, and eye-movements, 300-312
metabolic requirements of retina and,

648-659
toward moving objects, 342-352, 355, 362-
nodding, 342 [367, 390

parasitic (see parasitic fishes)
pelagic, 163, 380,382,392,429,449,528
photomechanical changes and, 150
position, 468
spectacle and, 449-461
swimming, 379-384
terrestrial (see terrestrial activity)
visual distances and, 247-288

TAXONOMICALLY:

lampreys, 158, 200, 371, 390, 555, 562

hagfishes, 391

elasmobranchs, 200, 372, 380-381, 429,

563, 568, 571
chondrosteans, 200, 569, 571-572
holosteans, 200

teleosts, 200, 303-305, 372-407, 431-436,
cladistians, 150, 200 [586

dipnoans, 150, 200, 223, 263, 590
amphibians, 150, 200, 305, 368, 418-419,

598-600, 605, 653
chelonians, 150, 200, 305, 422-423, 436-

438, 608, 611, 657
crocodilians, 150, 200, 305, 422, 436,

613-614, 657
Sphenodon, 150, 200, 616, 620-621, 657
lizards, 150, 200, 457-458, 622, 525-627,
chameleons, 306, 538 [633-634

geckoes, 201, 627
snakes, 150, 201, 458-459, 633-640
birds, 150,201,307-310,438-442,655-659
mammals, 201, 310-312, 442-448, 664-

665, 671, 675, 677, 684-689
Hadley, 540
Haempel, 481

INDEX AND GLOSSARY

747

hagfishes, hags (+ lampreys = cyclostomes)
eyes of, 210, 387, 562
habits of, 210, 391, 562
Hahn, 498

Haideotriton (amphibian: a cave sala-
mander), vestigial eye of, 407
halation, 229*

halfbeaks, ventral binocular field in, 293
Halichcerus (mammal: a seal), tapetum

lucidum of, 234
Halicmetus (teleost), spectacle of, 450
Halieutkhthys (teleost: a batfish), dual

pupillary opercula of, 222
Haller (see also muscle, retraaor lentis),

law or ratio of, 172
Hamburger, 487, 489
Hamilton, 499, 509
hammerhead shark: Sphyrna, q.v.
Hannover, 191; canal of, 7, 19*, 267,

681-682
Hapalemur (mammal: a lemurine),

diurnality of, 515
Hapale (mammal: marmoset)

cone: rod ratio in, 692 (entry for p. 686)
shape of fovea in, 190
Hapalidce (mammals: marmosets)
color vision of, 517
relationships of, 517
harbor seal: Phoca, q.v.
Harder (see glands)
hatchet -fishes : Gasteropelecus, Thoraco-

chorax, qq.v.
haw: nictitating membrane in mammals, q.v.
development of, 118
distribution of, 426-427
hawks

accommodation in, 280-281, 655

area and foveae of, 187, 307, 308-309,

661-662
bat-eating: Machctrhamphus; yellow iris

of, 545
cornea: retina areal ratio in, 289
distance-judgement of, 310
eye in, 280

size of, 642
eye- and head-movements of, 213, 308
habits of, 169-170, 197, 209
marsh- : Circus
retina of, 659
single cone of, 54
pecten in, 308, 649, 655-656

shadows of, 365
pupil responses of, 501
red-tailed: Buteo
fovea of, 182-183
pecten of, 649
retina in, 659

area of, 289, 656

scleral ossicles of, 441, 644

vision of, 366, 501, 661-662

visual acuity in, 209, 661-662

visual cells of, 54

oil-droplet colors in, 197, 502-503

visual fields of, 295, 307-309

visual trident of, 307-309
Hecht, 89, 502

hedgehog, European: Erinaceus, q.v.
Hein, 460

heliothermic: said of cold-blooded animals
which depend for warmth upon
direct sunlight
Helmholtz, 89 (see also Young-Helmholtz

theory)
Heloderma (reptile: Gila monster; escorpion)

ciliary muscle (lacking) in, 624

fixity of eyes of, 306

fovea (lacking) in, 625

habits of, 200, 458

lids of, 458

visual cells in

colorless oil-droplets of, 203, 627
HelodermatidcB (reptiles: a lizard family —

Heloderma + Lanthanotus) , 200
hemianopia, 336-337*

motion-perception in, 343
Hemidactylium (amphibian: four-toed sala-
mander), retinal summation in, 603
Hemidactylus (reptile: a spectacled gecko)

ciliary muscle (lacking) in, 624

Descemet's layers (lacking?) in, 623
hemoglobin, 63
hen, domestic: G alius, q.v.
Henschen, 522-523
Hering, 89, 464, 496, 513
herons, pecten in, 657
Herpele (amphibian: a ceecilian), eye

muscles lacking in, 606
Herpestes (mammal: mongoose), pupil of,
herrings et al: clupeoids, q.v. [221

Herter, 517

Hesperornis (extinct bird), 438
von Hess, 278-279, 467, 473-475, 477-480,
482, 485-487, 490-491, 494,
497-498, 503, 614
Hesse, organs of (in Amphioxus), 124-125,

126, 128
Heterodon (reptile: hog-nosed snake), spec-
Hilton, 533 [tacle of, 450
Himstedt, 490, 505
Hineline, 483
Hiodon (teleost: moon-eye)

adipose lids of, 383-384

tapetum lucidum (probable) in, 233
Hippocampus (teleost: sea-horse)

area centralis and fovea in, 187, 304, 306

falciform process in, 582

INDEX AND GLOSSARY

Hippopotamus
adnexa of, 443
compared with sirenians, 408
elevation of eyes in, 443
eyelashes of, 426, 443
habits of, 443
lid-movements of, 425
pupil of, 221, 443
taxonomic position of, 139, 676
vision of, 311, 408
Hogben, 535, 538

Holocephali (elasmobranchs: chimeeras)
habitat of, 392, 563
ocular shape in, 565
oculorotatory muscles in, 564
pupils of, 220, 222
retina in, 399-400

summation of, 568
sclera in, 416
tapetum (lacking) in, 240
taxonomic position of, 135-136
visual cells of, 568
Holostei (holostean fishes — Amia + Lepis-

osieus, qq.v.), 573-576
HomalopsincE (reptiles: a colubrid sub-
family— river snakes)
binocular field of, 293
elevation of eyes in, 438
spectacles of, 450
value of vision to, 293-294
homologous — homoiologous : homology con-
notes evolutionary derivation from
a common-ancestral strurture —
homoiology, evolutionary derivation
from non-contemporaneous portions
of a struaural substrate; thus: if
structures A and B (whether alike
in form and/or function or not)
were derived ancestrally from struc-
ture C, then A and B are homol-
ogous (with each other and with
C); but if A and B were derived
respeaively from strurture C and
from strurture D (D being an un-
modified descendant of C), then
A and B are homoiologous.
honey-birds, preference for red flowers by,
Honigmann, 498 [503

Hopkins, 510-511
Horio, 489-490

hornbill, ocular mobility of, 307
horned 'toad' : Phrynosoma, q.v.
horopter, 317*
horse

accommodation (lacking) in, 255, 285
color vision in, 505
eye of

ramp retina in, 255

size of, 171, 173, 211
fixation by, 3 1 1
gait of, 352

interpupillary distance of, 327
movement-perception by, 354 . ^

nirtitating membrane of, 427
optic axes of, 297
optic chiasma of, 319
pertinate ligament of, 680
pupil and iris of, 2 1 8, 227, 679
refrartion of, 287
retinal vessels of, 684
retrartor bulbi of, 420
taxonomic position of, 676
vision of, 246, 505
visual fields of, 289, 297-299, 354
Hosch, 589

Hottentots, visual acuity of, 190
Howell, 442-443

Hubbs, 202, 392, 402, 460, 548
hue: color in the strirtest sense — i.e., without
regard to variations in brightness
and saturation; thus: red and pink
are different colors, but the hue
of both is red
human eye (and vision; see also vision), 7-8,
10, 14-15, 27, 31, 35, 37, 39, 43-
44,47,54-55,82,87,91,94, 101-
102, 105, no-Ill, 173, 182, 194,
252,316, 321, 332, 335, 359,683
accommodation and refrartion of, 30-36,
31, 35, 272-273, 440, 285-287,
682-683, 689
refrartive errors, 26, 27-28, 194
adnexa of, 36-41, 37, 39
anomalous eyeshine of, 241
cornea of

biomicroscopy of, 452-453
relative area of, 289
dioptrics of, 29-30
fibrous tunic of, 672
fovea of, 7, 181-182, 190, 661, 689
interpupillary distance of, 327
lens, color of, 191, 199, 202, 204-205
movements of, 300-303
optic chiasma of, 47, 52
resolving power of, 207, 662
retina of, 43, 684
area of, 289
area of image on, 2 1 1
blind zone of, 289
summation of, 661
vessels of, 684
shape of, 672, 677

structure of, 6-22, 285, 674, 678-683, 689
visual angle of, 289, 297
visual cells of, 43, 54-55, 685-686, 688-
visual process in, 74-99 [689

INDEX AND GLOSSARY

749

hummingbirds

ares and fovea of, 187-188, 307
eye size in, 641
fundus and pecten of, 188
sensitivity to red of, 503-504
"von Husen, 658

Huso (chondrostean: a sturgeon), 136
Huxley, 139
hycEna (mammal: a canid), behavior of

pupil in, 156
hyaloid vessels: vitreal vessels (^.v.; and

see footnote, p. 575)
Hyborhynchus (teleost: a cyprinid), color

vision of, 486
Hydrochcerus (mammal: capybara; largest

rodent), pupil of, 221
Hydromantes (amphibian: a salamander),
complete terrestrial ity and vivi-
parity of, 368
Hydrophiinae (reptiles: sea-snake sub-family
of Elapidae)
accommodation and refraction in, 272-273
pupil in, 221, 228, 257, 272-273, 438,
Hyla (amphibian: a hylid anuran) [447
area centralis in, 305
complete terrestriality in, 368
dermal coFor changes in, 536
rhomboid pupil in, 223
HylidcB (amphibians: common tree-toad
family)
habits of, 368, 418
pupils of, 223-224
scleral cartilage in, 595
visual cells in, 598-599
Hymenal aimus (bird: New Zealand blue
duck), frontality and binocular
fixation of, 295
HynobiidaB (amphibians: a urodele family)
relationships of, 600-601
sclera in, 601
hypermetropia, 27*, 27, 252-253
distribution of, in animals, 273
Hyperolius (amphibian: an anuran), pupil
pupil of, 223, 692 (entry for p.
223)
Hypogeophis (amphibian: a caecilian), eye

of, 605-606
Hypopachus (amphibian: an anuran)
scleral bone in, 274, 595
vertical pupil in, 223
Hypsiglena (reptile: a colubrid snake)
fibrous tunic of, 628
visual cells of, 63, 216, 638-639
rhodopsin (lacking) in, 168
Hypsignathus (mammal: a fruit-bat), ret-
inal tapetum lucidum of, 684
Hypsiprymnus (mammal: a kangaroo),
conus papillaris of, 672

Hyracoidea (mammals: hyraxes or conies),
taxonomic position of, 676

hyrax: Procaria, q.v.

Hystricidae (mammals: a rodent family),
eyeshine and possible tapetum
lucidum in, 230, 241

I

Ichthyococcus (deep-sea teleost), develop-
ment of tubular eye in, 400
Ichthyomyzon (cyclostome: a lamprey)

size of eye in, 556

visual cells of, 560-561
Ichthyophis (amphibian: a caecilian), eye

of, 605-606
Ichthyopsida : cyclostomes -I- fishes -i- am-
phibians
Idiacanthus (deep-sea teleost), adult and

stalked larval eyes of, 403-405, 404
Iguana (reptile: an iguanid lizard)

lens of, 620

ocular proportions in, 617

retina of, 625

visual fields in, 294
Iguanidas (reptiles: a lizard family)

dermal color changes in, 538-542

eye-movements in, 538-542
illicium, 548*
lUysiidae (reptiles: a primitive snake family)

habits of, 201

pupils of, 220
Impennes: penguins, q.v.
India, visual acuity among natives of, 190
Indrt (mammal: a lemurid), 692 (entries
for pp. 221, 228)

diurnality of, 228, 515

iris color in young and adult of, 550

pupil of, 221
Indris, black: Indri, q.v.
Indrisinas (mammals: a lemurid sub-family),

diurnality in, 515
induction, 499* (see after-image, color-
contrast )
Insectivora (order of mammals: moles,

aquatic, 443 [shrews, etc.)

binocularity of, 310

as 'bottle-neck' forms, 284, 520, 675, 687-
689

color vision in, 517

habits of, 201

nictitating membrane in, 426

optic axes of, 297

primitive, eyes of, 687

pupils of, 221

relationships of, 135, 139, 504, 517, 675-

size of eye in, 677 [676

upward tilt of eyes in, 296

visual cells of, 685

750

INDEX AND GLOSSARY

intensity (objeaive; cf. brightness)
adaptations to, 143-246

dermal, 530-532
adjustment of pupil to, 265, 592
discrimination of, 70, 72*, 485
vs exposure-time, 230
fusion and, 70, 72
photochemical effect of, 103
reference of brightness to, 247
regulation of, 469
inter-pupillary distance

in man and mammals, 327
in relation to bathopsis and stereopsis,
327, 330, 405
intoxication, disturbance of reflex eye-
movements in, 301
invagination: an in-bulging or in-pocketing
invertebrates: animals (except lower chord-
ates) lacking a vertebral column
blind, 388, 390
photophores of, 396, 402
visual organs of, 2-3, 254, 257, 268, 282,
343, 351, 370-371, 395, 492, 324
inward convergence of retina: summation, q.v.
iodopsin, 100*, 102
Ipnops (deep-sea teleost)
photophores of, 398
unique complete eyelessness of, 397-398
iridocytes, 526*, 533, 581, 595, 619, 630,
iridosomes, 526*, 597 [679

iris (see also pupil)

argentea of, 159, 236, 558, 567, 571-572,

575, 577, 584
circulation of, taxonomically:
lampreys, 558
elasmobranchs, 566
teleosts, 584
amphibians, 598, 602
crocodilians, 619
Sphenodon, 619
lizards, 619, 624, 630, 647
snakes, 630
birds, 647

mammals, 14-15, 673
coloration of, 16-17, 543-551, 545, 547,
584, 614, 668, 679
changes of, 549-551
sexual differences in, 226, 549-550
elimination of, 401
folds of, 276, 564, 567, 596
muscles of, 153-163

role of, in accommodation, 285, 436-
438, 437, 440-441, 444, 622,
647-648
'sphinrter of Grynfeltt', 160*, 584
voluntary (?) control of, 156, 269
taxonomically:
elasmobranchs, 567-568, 571

teleosts, 160, 584

amphibians, 597, 602

sauropsidans in general, 269-270

chelonians, 436-437, 610, 614

crocodilians, 614

Sphenodon, 619-620

lizards in general, 624

geckoes, 223

snakes, 438, 630, 635

birds, 156, 269, 440-442, 441, 647

mammals in general, 218, 444, 619-

620, 647, 668-669, 673, 678-679
seals, 446-448
man, 10, 15, 17-18
photomechanical changes of, 150

(Table II)
physiology of, 17-18, 153-163, 217-228,

590
taxonomically:
lampreys, 158, 558, 572
elasmobranchs, 567-568
sturgeons, 571-572
holosteans, 574-575
teleosts, 580, 584
dipnoans, 590
anurans, 596-598
urodeles, 602
cscilians, 606
chelonians, 609-610
crocodilians, 614
Sphenodon, 617-620, 647
lizards, 624, 647
snakes, 630, 633, 635
birds, 156, 269, 647
monotremes, 667-668
marsupials, 673
placentals, 156, 669, 678-680
man, 14-15, 16-18
isabelline: pale in coloration as a conse-
quence of partial albinism
birds, ostracism of, 466
Ischreyt, 440
Isely, 524

isodynamic cells, 322*
Ixobrychus (bird: a bittern), binocularity
and freezing posture of, 309

Jacobson, organ of, 424*

Javal, 315

Johnson, 249, 286, 292, 296, 312, 447

Jokl, 657

Joseph, cells of (in Amphioxus) , 120, 126,

128
]ulis (teleost: a labrid)

binocular field of, 292

fovea of, 304
jumping hare: Pedetes, q.v.

INDEX AND GLOSSARY

751

Kahmann, 292-293, 304, 497, 681-682

Kajikawa, 650, 655

kakapo: Strigops, q.v.

Kalischer, 506-507

kangaroos (mammals: highest marsupials)

color vision in, 518

conus papillaris in, 672

cornea in, 671

ecology of, 664, 686

evolution of, 283

habits of, 201, 227, 518, 686

lens size and shape in, 673-674

ocular proportions in, 671, 673

oil-droplets of, 201, 203

pupils of, 221, 227

taxonomic position of, 664
kea: Nestor, an Australian parrot; alleged

feeding habit of, 657
Keeler, 511
Kerr, 591
keystoning, 317*

killifishes: Fundulus, Cyprinodontidee, qq.v.
kinaesthesia : sense of movement and positions

of parts of the body
kingbird, 209
kingfishers (see also Alcedo)

accommodation in, 273, 442

areae and foveje of, 187, 307, 442

feeding method of, 439

oil-droplet colors in, 198, 502-503
Kinnaman, 515
Kinosternidae (reptiles: musk-turtle family),

sensory guidance of, 437-438
Kittredge, 505
kiwi: Apteryx, q.v.
Klauber, 230
Kleinholtz, 542
Kliiver, 515
K6hler, 515
Kblliker, 525
K5nig, D., 274, 437
K6nig, A. 91
Kogia (mammal: pygmy sperm whale),

relationships of, 412
Kohts, 515
Kolmer, 442, 481, 664-665, 667, 671, 678,

685-686
Kolmer-Held, fiber of, 55, 58
Kolosvary, 510, 514
Korte, laws of, 360
krait: Bungarus, q.v.
Krause, A. C, 75
Krause, W., 215, 497
von Kries, 64
Kiihn, 487
Kuhne, 74, 100
Kurz, 534

Labrax (teleost: a labrid), divided chorioid

gland of, 581
Labridffi (teleosts: wrasses)

binocular field in, 292

falciform process in, 582

side-resting habit in, 385
Labrisomus (teleost), stripes crossing iris in,
labyrinth, membranous (of ear) [546

development of, 129-130

eye-movements and, 301
Lacerta (reptile: a lacertid lizard)

ciliary muscle in, 619, 624

color vision in, 495-496

optomotor reartion and, 492

embryo of, 271

excursion of eye in, 306

transversalis muscle in, 278

visual fields of, 294
LacertidcB (reptiles: a lizard family), lid

windows in, 457
Lacertilia: lizards, q.v.
lacrimal system (see also glands),

taxonomically:

amphibians, 419

chelonians, 423

crocodilians, 422

Sphenodon, 421

lizards, 423
spectacled, 424

snakes, 424

birds, 425

mammals, 426, 443
seals, 445
man, 39, 41
lacus lacrimalis, 40*
Ladd-Franklin, 464
ladyfish: Albula, q.v.
Lamar gus (elasmobranch: a deep-sea shark)

eye of, 398

peculiar sclera of, 565

tapetum lucidum (lacking) in, 243, 398,
568
Lagomorpha (order of mammals: rabbits,
hares, pikas)

ciliary processes in, 681

eyeshine in, 230, 241

meduUated portion of retinal nerve-fiber

optic axes of, 297 [layer in, 684

pupils of, 221

retinal vessels of, 684

taxonomic position of, 139, 676

visual fields of, 296
lamina vitrea: glass membrane, q.v.
Lamna (elasmobranch: porbeagle shark)

cones in, 692 (entries for pp. 561, 568)

pupil of, 222

verticality of cornea in, 381

752

INDEX AND GLOSSARY

Lampanyctis (deep-sea teleost), retina of,
Lampetra (cyclostome: a lamprey) [399

accommodation and refraction of, IJl-lJi

'annular ligament' in, 557

chorioid of, 558

dermal rhythm in, 538

eye and surroundings in, 557

optic nerve of, 559

retina of, 559

visual cells of, 559, 561
lampreys (+ hags = cyclostomes), 557

accommodation and refraction in, 258-
260, 265, 268, 272-273

'annular ligament' in, 557

chorioid in, 558

color vision (?) in, 518-519

comparison with lungfishes, 590, 604

cornea in, 459, 557

perpetual contact of lens with, 259

corneal muscle of, 556-557

dermal color changes in, 537-538

development of eye in, 117-118, 126, 127,
131, 406-407

ependyma in, 128

habits of, 158, 200, 371, 390, 555, 562

intra-ocular fluids of, 371

iris in, 158, 558, 572

lens in, 557, 559-560

yellow coloration of, 191, 199-200

macrophthalmia stage of, 406-407

median eyes of, 338- 339

oculorotatory muscles in, 556, 564, 574

optic chiasma of, 320

optic nerve of, 559-560, 569

orbit of, 556-557, 565

pia mater of, 119

pupils of, 158, 220

retina in, 177, 518, 559-562
development of, 117-118

rhodopsin in, 562

sclera in, 556-557

size and shape of eye in, 556-557

spectacle of, 258, 380, 449-452, 451,
459, 556

taxonomy and life-cycles of, 135-136, 555

visual cells of, 56, 58, 176, 559-560,
561-562, 688

visual field of, 291, 320

vitreous of, 259, 560

water balance of, 371
Lam pro pel tis (reptile: king snake)

adaptations for sensitivity in, 168

conus papillaris of, 631

visual cells of, 638
Langmuir, 351

Lankester, eye-origin theory of, 121
lantern-fishes: Myctophidae, Sternoptychidae,
Lashley, 498-499 [qq.y.

laterality, 290-291*

development of, 444

imposed, 299, 413

pupil size and, 386
lateral geniculate body, 329*, 334-335,

337-338, 522
lateral line system (of sense-organs),

124-125*, 129-130, 271
Latimerla (only known living crossopter-

ygian), 136, 263, 589-590, 604
Laurens, 496, 501, 537
leaf-footed lizards: Pygopodida, q.v.
LeBlond, 88
Lebistes (teleost: guppy), dermal color

changes in, 534
Leinfelder, 312
Lemmrich, 644
Lemur (mammal: a lemur)

area centralis in, 187, 245, 523

cerebral 'color cells' in, 523

color vision in, 515-516, 521, 523

eyeshine in, 230, 241

habits of, 201, 515, 521

pupil in, 221, 228

tapetum lucidum in, 241, 245

visual cells of, 685
Lemurin£e (mammals: true lemurs),

habits in, 515
Lemuroidea (mammals: -f Anthropoidea =
Primates; Prosimije; 'lower'
primates, ^.v.)

area centralis in, 187, 245, 523

color blindness of, 515-516, 521

frontality of, 331,413

habits of, 201, 515

immobile eyes in, 413

pupil in, 221, 227-228

relationships of, 516-517

retina in, 216, 685

degeneration of, in captivity, 228

tapetum lucidum and eyeshine in, 233,

tubular eyes in, 212-213 [241,517

shape of ciliary body in, 286

visual cells of, 685
lemurs: Lemurids

in strictest sense: Lemurins
lens (see also accommodation, refraction)

action of, 23-24, 25-26

annular pad ('Ringwulst') of, 275, 276*,
284, 609-610, 624, 630, 632, 647,
648, 655, 669, 674

anterior pad of, 628, 630*, 633

asymmetric, 434-435, 442

bifocal, 257

coloration of, 191, 199-205, 443, 515

contact-, 441

development of, 105-106, 109-110, Ill-
dispersion by, 194 [113, 648

INDEX AND GLOSSARY

753

embryonic circulation of, 112-113
epithelium

special extent of, 446

special function of, 648
evolutionary origin of, 129-133
fibers, formation of, I 1 0- 1 I I
flatness index (diameter divided by thiclc-

taxonomically: [ness) of

fishes and amphibians, 266, 432, 435,

chelonians, 610, 620, 669 [597, 602

Alligator, 620

Sphenodon, 620

lizards, 620, 624

snakes, 630

birds, 642, 647

monotremes, 669

marsupials, 674

anthropoids, 669, 683

sirenians, 409

whales, 414, 683

seals, 445, 683
fluorescence and absorption of ultra-violet
location of, 592-593 [by, 196, 375

migration of, 401-403
movement, consequences of, 265, 442
placode, 106, 109*-l 10, 124-125, 129-130
refractive index of, 29, 160, 265, 436, 647
regeneration of, 130-131
relative sizes and shapes of, 173, 212-214,
563, 590, 601-602, 673-674,
683-684
softness of, 436-438, 440, 610, 624, 647
spherical, 213-214, 407, 409, 445-446,

604, 610, 683-684
spherical aberration of, 156, 160, 211
suturing of, 20, 110-112, III
taxonomically:

lampreys, 191, 199-200, 557, 559-560
elasmobranchs, 200, 255, 563, 564-565
chondrosteans, 570
holosteans, 575
teleosts, 185, 213, 261, 387, 400-401,

431,433-434,454,577,583
dipnoans, 590

amphibians, 266, 592-593, 597, 601-602,
chelonions, 277, 437, 609-610 [606

crocodilians, 614
Sphenodon, 618-620

lizards, 173, 200-201, 623-624, 630, 632
snakes, 186, 201, 282-283, 438, 456, 630-

631, 628, 633
birds, 173, 213, 441, 643, 645, 647-648
monotremes, 667, 669
marsupials, 173, 673-674
placentals, 173 201, 213, 255, 409, 413,
446, 678-684, 683

man, 7, 10, 19-22, 31, 194
ienticonus, anterior, 436*-437

lentiflavin, 199*, 515, 518
leopard frog: Rana pipiens, q.v.
Lepidosiren (dipnoan: South American
lungfish), 136

dermal color changes in, 525, 537

eye of, 263

oculorotatory muscles of, 589

optic nerve of, 591

pigment epithelium of, 590

pupil of, 223

retinal photomechanical changes (claimed

visual cells of, 216, 591 [for), 223

vitreal vessels of, 653
Lepisosteus (holostean: gar)

annular ligament of, 574-575

chorioid of, 574

falciform process (?) in, 575, 582

iris of, 575

lens of, 575

lens-muscle papilla of, 264, 273, 575

optic nerve and disc of, 576

relationships of, 137

retina of, 200, 576

sclera of, 574

size and shape of eye in, 381, 574
leptocephalus, 406*
Lepomis (teleost: a centrarchid)

annular ligament of, 581

color vision in, 484-486

cornea of, 580

twin cone of, 59
Leptodeira (reptile: a colubrid snake)

closable pupil of, 162, 166

retina of, 167, 638

rhodopsin in, 166

visual cells of, 638, 640
Leptophis (reptile: a colubrid snake), optic

axes of, 294
Leptotyphlopida (reptiles: a fossorial snake

eyes of, 627 [family)

spectacles of, 450
Lepus (mammal: European brown hare),
habits, vision, anterior blind
field of, 296
Leuckart, law or ratio of, 174*, 346
Leydig, 542, 589
Lichanotus (mammal: an indrisine lemur),

nocturnality of, 515
Lichanura (reptile: California rosy boa)

canal of Schlemm in, 629-630

ciliary body of, 629

scleral pigment in, 628
Lichia (teleost: a scombroid), binocular

field of, 292
lids (see also nictitating membrane, spectacle)

adipose, 118, 381-384, 382-383
'imperforate', 459
as source of spectacle, 383, 450, 460-461

754

INDEX AND GLOSSARY

lids — cont'd

aperture of — orientation etc., 38-40, 422-

424, 428, 641, 644
blinking reflex of

in birds, 644

cause of, 40-41

speed of, 40, 425

substitute for, 427
development of, 115, 117, 436, 452
effects of, on eyeball struaure, 428
as source of spectacle, 423
tarsal plates of, taxonomically:

chelonians, 422

crocodilians, 421-422

Sphenodon, 420-421

lizards, 423

birds, 424

mammals in general, 425-426, 665

whales, 412

seals, 445

man, 39-40
temporary, 431-432, 452, 578
vertical (see adipose, above)
'window' in, 423, 440, 450, 457
taxonomically:

elasmobranchs, 382, 386, 428-429, 563
amphibians

aquatic, 407, 419, 593, 601

terrestrial, 419, 423, 430, 436, 593, 601
chelonians, 422-423, 450, 457
crocodilians, 421-422
Sphenodon, 42 1
lizards, 423, 457-458
birds, 424-425, 644
mammals, 425-427, 443-445, 665

sirenians, 408

whales, 413-414

seals, 444-445

man, 38-41, 39
Lieben, 535
ligament

annular, 159-160*, 574*, 580*, 604

taxonomically:

lampreys, 557, 574

sturgeons, 570, 574

holosteans, 574

teleosts, 577, 580-581, 584
pectinate, 275, 278*, 280, 557, 596, 613,
629*, 645-648, 668, 679-680*, 683
suspensory (of lens; see also zonule)

taxonomically:

elasmobranchs, 564, 567

sturgeons, 571, 575

holosteans, 575

teleosts, 261, 577, 583
tenacular: restraining

of ciliary body, 275, 280, 645

of eyeball, 578

light (see also color, spectrum)

absorption of: the reception of light in a
material and its conversion into
radiation of longer wavelengths
(usually 'heat' — infra-red 'light');
absorption and fluorescence are
essentially the same phenomenon;
cf. fluorescence, below.
in deep-sea environment, 393-403
dispersion of (see chromatic aberration)
fluorescence of: the reception of short-
wave (usually ultra-violet) light
in a material and its re-radiation
at longer (usually visible) wave-
lengths; differs from 'absorption'
only as to the portion of the grand
spectrum involved; 375, 488-489
infra-red

absorption of, by water, 373
photography with, 197
visibility of, 502
interference of: a phenomenon occurring
in extremely thin films of reflective
material, wherein light rays reflect-
ed from the top and bottom sur-
faces of the film are variously out
of phase, resulting in cancellation
of some wavelengths and reinforce-
ment of others, so that the reflected
light is colored though the incident
light be white and the film devoid
of differentially-absorbing (colored)
substances; 231, 526, 543
nature of, 1-2*

—producing organs: photophores, q.v.
properties of water toward, 369, 373-379,

462, 488-489
reflection of (see also tapetum lucidum)
critical angle of, 3 77* -3 78
under water, 375-376
refrartion of, 22*, 22, 23-24, 265
scattering of, 195, 197
as sensation, 1-2
ultra-violet, 473*

absorption of, in ocular media, 196
absorption of, in water, 373, 375
harmfulness of, 196, 375, 417, 524
visibility of, 488-489, 515
light-cells (of brain), 522-523
lighdess habitats, 209-210
limicolous: mud -dwelling
limitans: external limiting membrane of
lion (a felid) [retina, q.v.

American: cougar, q.v.
eye and vision of, 145, 245-246
tapetum lucidum of, 145, 234, l^'J-l^S

lionfish: Pterois,

lipid, lipoid: of fatty nature

INDEX AND GLOSSARY

755

lipophores, 526*, 630, 647, 679
Lipotyphla (mammals: division of insecti-
degenerate eyes in, 677 [vores), 676*
pure-rod retinje in, 685
Lissamphibia: Amphibia excepting Stego-
Lister, 535 [cephali

Listing, laws of, 302
littoral: living in the water over shores and

beaches
lizards (sub-order Lacertilia of reptilian
order Squamata)
accommodation and refraction in, 251,

254, 270, 272-273, 275-276, 623-
activity of, 611, 653 [624,632

adnexa of, 423-424, 457
chameleons, 289-290, 306
compared with Sphenodon, 617
spectacles, 450-451, 456-458, 457
amphibious, 438
area centralis and fovea in, 173, 184, 187-

190, 306, 625, 632
binocular vision in, 299-300, 306, 321
blind, 458 (see also worm-lizards)
chorioid of, 617, 623
ciliary body of, 276, 618-619, 623-624, 632

muscles of, 279-280, 623-624, 646
color vision in, 102, 193, 495-497, 519-
coloration of eye in, 546-549 [520

compared with Sphenodon, 617-618,

622-623
conus papillaris in, 611, 624-625, 631-

632, 650, 653-654, 656
cornea in, 617, 623
critical fusion frequency in, 72, 520, 692

(entry for p. 72)
dermal color changes in, 466, 538-543
distribution of, 622

embryo of, showing corneal sensillae, 271
eye-movements in, 299-300, 306
fossorial, 625, 635 (see also worm-lizards)
habits of, 145, 150, 162, 168, 200-201,
203-204, 206, 215, 293, 306, 342,
438, 450, 457-458
iris of, 624, 630, 647
lens in, 173, 623-624, 630, 632

yellow coloration of, 191, 199, 201,
nasad asymmetry in, 300 [203-204

ocular proportions in, 162, 173-174, 300,

623, 632, 642
ocular resemblance to birds, 641
optic axes in, 294
optic nerve of, 632
origin and relationships of, 134-135, 138

relation to snakes, 138, 632-636
parietal eye in, 339-340
perception of motion by, 344
pupils of, 150, 161-162, 166-168, 176,
220, 223-224, 256, 273, 289

retina in, 162, 178, 611, 620, 623, 632

photomechanical changes of, 150
sclera in, 623

ossicles of, 271, 274, 617, 623, 632
transversalis muscle of, 278-279, 299-300
visual acuity of, 162, 170, 206, 306
visual cells of, 56, 62-63, 161, 167-168,
176, 178, 200, 216, 254, 520, 621,
625-627, 626, 632, 638, 653
oil-droplets of, 102, 192-193, 200-201,
rhodopsin in, 162, 168 [203

visual fields of, 289, 293-294, 306, 321
vitreous of, 624
zonule of, 624, 646
llama (mammal: a tylopod), interpupillary

distance of, 327
local signs of direaion, 318*, 328, 330,

347-348
Locher, 513-514, 517
Lonnberg, 534

Loken, 692 (entry for p. 99)
Loligo (mollusc: a squid), eye of, 3
Long, 507

look-down: Vomer, q.v.
loons

accommodation in, 440

Crampton's muscle in, 441
nictitans-lens in, 440
ringwulst of, 647
swimming habits of, 439
Lophiomus (teleost: a batfish), larvoid

illicium of, 548
Lophius (teleost: angler)
elevation of eyes in, 432
falciform process (lacking) in, 582
habitus of, 385
mobile pupil of, 160
temporary lids of, 432
vitreal vessels of, 582-583
Lophopsetta (teleost: sand dab), dermal
color changes of, 482, 530
lorises (slow-moving lemurs)
color blindness of, 520
pupils of, 228
Lota (teleost: only freshwater gadid; burbot)
habits and cone: rod ratio of, 176
spectacle of, 450
louvar: Luvarus, q.v.
Lubbock, 506
Lucifuga (teleost: a cave brotulid), history

of, 388
Lucioperca (teleost: a percid), occlusible

tapetum lucidum of, 236-237
luminous shark: Etmopterus, q.v.
lungfishes: Dipnoi, q.v.
Luscinia (bird: nightingale), pecten of, 656
Lutianus (teleost: snapper), color vision
of, 473. 476

INDEX AND GLOSSARY

Lutra (mammal: a mustelid carnivore; otter)

accommodation and refraction of, lll-iyi,

adnexa of, 444 [444

habits of, 443-444

iris of, 678

sphincter pupillae of, 444, 447

pupil of, 162
Luvarus (teleost: louvar), guanin in retina

of, 585
Lygodactylus (reptile: a diurnal gecko)

pupil of, 203, 220, 627

visual cells of, 203, 627

yellow lens of, 199, 201, 203
Lygosoma (reptile: a scincid lizard), lid

window of, 450
Lymnomedusa (amphibian: a hylid anuran),

vertical pupil of, 223
lynx (a felid)

cornea of, 214

eye of, 1 73
lysozyme, 41*

M

M abut a (reptile: a scincid lizard), head of,

showing lid window, 457
macaques (lowest catarrhine anthropoids),

color vision of, 515
macaw, color change in, 525
McEwan, 576, 586
Machterhamphus (bird: bat-eating hawk),

yellow iris of, 545
mackerels (see Scomber, scombroids)
Macrochiroptera, 692 (entry for p. 254)
Macropodidie: kangaroos and wallabies, qq.v.
macrophthalmia, 406-407*
MacTopus (mammal: a kangaroo), eye and

lens of, 673-674
Macrorhinus (mammal: elephant seal)

ballasting habit of, 440

change of optic axes in, 444

eye of, 445

lid movements of, 425

terrestrial myopia of, 448
macula (lutea), 181*

decussation of, 319

pigmentation of, 99, 183, 191, 204, 477

sensitivity of, 185

substitute, 322, 330
magpie, color-interest of, 466
Malacopterygii: soft-rayed teleosts; 391*,

adipose lids m, 383 [576*

characteristics of, 391-392, 576

double (?) cones in, 586

guanin tapetum lucidum in, 236

ocular chararters of, 576-578

spectacles in, 460-461
Malpolon (reptile: a colubrid snake)

visual acuity of, 178, 637-638

visual cells of, 178, 637-638

visual fields of, 294
Mammalia (monotremes + marsupials -i- pla-
centals, qq.v.), 138-139*, 663-689
man-eating shark: Carcharodon, q.v.
manatee: Trichechus, q.v.
mandrill, normal myopia of, 286
mangabey: Cercocebus, q.v.
manipulation and binocularity, 312
Manis (mammal: scaly ant-eater), nictitat-
ing membrane of, 426
Mann, 546, 619

Mantd (elasmobranch: a ray), pupil and
horizontal aim of eyes in, 385-386
mantas: Mobulidse, q.v.
Mantipus (amphibian: an anuran), eyespots

on skin of, 544
mantis, protective coloration in, 524
marine iguana: Amblyrhynchus, q.v.
Marmosa (mammal: mouse opossum)

ciliary muscle of, 673-674

cornea of, 671

eyeshine in, 238

pigment epithelium of, 44

retinal vessels of, 672

tapetum lucidum (lacking) in, 238

visual cells of, 670
marmosets: Hapalidae, q.v.
Marmota (mammal : a sciurid rodent;

habits of, 209 [woodchuck)

hypothetical color vision of, 468-472

optic disc of, 180
marmots: marmotine sub-family of Sciuridce;
includes ground-squirrels (Citellus)
and prairie-dogs (Cynomys, q.v.),
but NOT Marmota

area centralis in, 187

eye mobility in, 312

pupils of, 221

and visual field, 299

visual acuity of, 312

visual cells of, 176
marsupial mammals (see also kangaroos, wal-
labies, phalangers, opossums)

ciliary body of, 673, 681

color vision in, 518

conus papillaris in, 654

development of, 663

eye-movements in, 310-312

eyes of, 173, 670-675, 673-674, 686-687

eyeshine and tapetum lucidum in, 143,
233, 238-241, 239, 672

habits of, 201, 227, 518, 664

optic axes of, 297

optic chiasma in, 52, 319

origin and evolution of , 135, 138-139,284,
663-664, 671, 675, 686-687

pupils of, 143, 221, 227

INDEX AND GLOSSARY

757

retina in, 143, 239, 674-675

circulation of, 201, 239, 654, 672
visual acuity in, 207
visual cells in, 59, 670, 675, 685, 688
oil-droplets of, 201, 203
martens: Martes, q.v.
Martes (mammal: a mustelid carnivore)
habits of, 170
sensory capacities of, 508
Mast, 482, 527

Masticophis (reptile: whip-snake), pupil of,
mastiguve-.U Tomastix, q.v. [Ill

Mastodonsaurus (amphibian: stegoceph-

alian), reconstruaion of, 137
Matthews, 502

Matthiessen, ratio of, 262*, 446
matutinal: pertaining to morning hours;
Mayerhausen, 291 [auroral

median eyes, 126-127, 129, 137, 338-340,

339, 634
Megachiroptera (mammals: chiropteran sub-
order; fruit-bats or 'flying-foxes'),
692 (entry for p. 254)
mammillated chorioid of, 254-255, 270,

273, 678
retinal degeneration in, 228
retinal tapetum lucidum of, 238, 241, 684
visual cells of, 685
Megalobatrachiis (amphibian: Japanese
giant salamander)
accommodation (lacking) and vision of,
scleral cartilage of, 601 [267-268

vascular cornea of, 602
visual cells of, 603
melanin: a pigment (or group of pigments),
dark brown or black in color, which
is characteristic of animal tissues
and which is under genetic control
— its absence being albinism
melanophores, 526*, 581, 597
Melopsiltacus (bird: Australian zebra grass-
parakeet; budgerigar), color vision
of, 499-500
Melursus (mammal: a bear), false blink

in, 427
meninges: the protertive and nutritive mem-
branes which cover the brain and
spinal cord — the dura mater (outer)
and the pia-arachnoid sheath (in-
ner); 119, 133, 452
Menner, 365-367, 685
Menotyphla, 676*
mergansers

feeding habits of, 439
accommodation and, 441
Merker, 488, 515

mesoderm: intermediate cell-layer or -mass
of an embryo (seeeao-, endoderm)

mesothelium: a sheet or layer of cells of
mesodermal origin (c/. epithelium)
Metriorhynchidae (reptiles: an extinct croco-
dilian family), scleral ossicles in,
274
Microchiroptera (mammals: small-bat sub-
order), eyes and vision of, 255
Microhylidae (amphibians: an anuran family)
oil-droplets (lacking) in, 599-600
scleral bone in, 595
MicTopterus (teleost: a centrarchid ) , eye-
color change in anoxia in, 551
Mkroscalabotes (reptile: a lidded gecko),

pupil and visual cells of, 627
minimum separabile, 207*
mink, red-curiosity of, 466, 508
minnows: Cyprinidee, q.v.
Misgurnus (teleost: giant loach), branched

optic nerve of, 367
mitochondria: tiny, lipoid formed elements
in the cytoplasm of most kinds of
cells
Mobulidae (elasmobranchs: a batoid family;
aim of eyes in, 386 [mantas)

pupils of, 220, 222, 386
moccasin: Agkistrodon, q.v.
mole-rats: Spalax, Ellobius, Bathyergidse,

qq.v.; eyes of, 687
moles

eyes of, 210, 677, 687
fossorial habit of, 209
lids of, 458

marsupial: Notoryctes, q.v.
taxonomic position of, 676
Mold (teleost: ocean sunfish)
size of eye of, 415
corneal laminations of, 580
moment, biological, 351*, 364-365, 588
Monacanthus (teleost: filefish), eye-move-
ments, pupil, and possible fovea of,
304-305
monitors: VaranidcE, q.v.
monk-fish: Squatina, q.v.
monotreme mammals: Ormthorhynchus,
Tachyglossus, Ziglossus, qq.v.
ciliary body in, 667, 681
eyes of, 664-671, 667, 686
eyeshine in, 240

habits of, 201, 203, 227, 664, 686-687
nictitating membrane in, 426, 665
optic axes of, 297
origin and evolution of, 135, 138-139,284,

663-664, 666, 669, 671, 675
pupils of, 221, 227
retina in, 654, 669-671
visual cells in, 201, 670-671, 675, 686, 688
oil-droplets of, 201, 203, 692 (entry for
moon-eye: Hiodon, q.v. [p. 203)

758

INDEX AND GLOSSARY

Moore, 188, 236

Mordacid (cyclostome: a lamprey),

relationships of, 555
Mormyridae (teleosts: elephant-fish family)
chorioid gland (lacking) in, 581
falciform process (lacking) in, 582
guanin in retina of, 585
pseudobranch (lacking) in, 581
scleral cartilages of, 578
spectacles of, 450
visual-cell bundles of, 588
vitreal vessels of, 582-583
Moroni, 535
Moras (bird: gannet)

circular ciliary muscle in, 273, 441
depth of swimming of, 226
distance-judgement of, 310
feeding method of, 439
fovese of, 310
mosasaurs: extinct reptiles; 138
Motacilla (bird: wagtail), retina of, 661
motion pictures
basis of, 358-361
seen by animals, 362
mouse, European long-tailed field-: Apo-
mouse, house- [demus, q.v

color vision in, 510-511
extent of cornea in, 214
eye of, 173

protrusion of, 426
lens of, 1 73, 674
lid movements of, 425
optic axes of, 297
optic disc of, 179
mouse, red-backed: Clethrionomys, q.v.
movement and its perception
apparent

autokinetic, 347*

stroboscopic (= ^i-phenomenon), 356-

365, 357, 359, 367
of whole field, 301, 348
avoidance of, 312
grades of, 345-347

sensory basis of, 349-365
perception of, 247, 303, 342-367
accommodation and, 366
adaptation and, 352-356
avian pecten and, 365-367, 651
barrel distortion and, 354
in center vs periphery, 352-356
motor factors in, 348-349
pathology of, 364
primitiveness of, 343
real vs apparent, 361-362
relativity of, 347-349
in scotomata and hemianopia, 343
sensory factors in, 349-367
threshold of, 347. 350

referred, 349*

saliency of, 343-344, 353, 355-356
toward-, 344
movingness, 346* -347, 351*; in animated

cartoons, 360
mud-minnow: Umbra, q.v.
mud-skippers: Boleophthalmus, Periophthal-

mus, qq.v.; spectacles in, 450
MiiUer, D., 508
MiJller, H., muscle(s) of

(circular) of ciliary body, 10, 32-33*, 280

distribution of, 272-273, 285-286, 441
of human upper lid, 39*, 39
(meridional), special, of avian ciliary
body, 280*, 646
Note: Still a fourth 'muscle of
Miiller' occurs as a vague sheet
of smooth fibers in the mammal-
ian orbit
Miiller, J. (see also Newton-Miiller-Gud-
Muenzinger, 509 [den), 291

Mugil (teleost: mullet)

aerial vision and adaptations therefor in,
color vision in, 476-477 [435-436

visual cells in, 586
mullet: Mugil, q.v.
Munn, 509

Murex (mollusc: a snail), eye of, 3
Muridce (mammals: mouse family of
ciliary muscle in, 285, 680 [rodents)

degenerate eyes in, 677
eyes of, 680
lacrimal system in, 426
optic axes in, 297
vision of, 288
Murphy, 226

Murray turtle: Chelodinct, q.v.
murres, ringwulst in, 647
Mus (see mouse, house-)
muscles (see also Miiller, H.)

Briicke's: principal, meridional ciliary

muscle; see ciliary muscle (below)
bursalis [and Briicke

in birds, 270, 420-421, 424, 642
derivation of, 642
in lizards, 421, 423
retractor of, 421
of chorioid, 281, 442, 645
ciliary (of Briicke, Crampton, and Miil-
ler), 261-263, 267, 269-270, 272-
273 (Table VIII), 277-278, 279-
282, 284-288, 409, 414, 437, 441
445, 583-584, 592, 595-596, 602
609-610, 614, 618-619, 623-624
632, 645-646, 665, 673-674, 679
corneal, 258-259, 556 [680

depressor (of lower lid), 425, 644
'E', 564

INDEX AND GLOSSARY

759

of iris (see iris, muscles of)
levator bulbi, 419, 432, 594

derivative of, 606
levator of upper lid, 40, 425, 644
masticatory, as source of levator bulbi, 594
oculorotatory (see also eye-movements)

absence of, 606

accommodation and, 259-260

control of, 329-331

derivatives of, 422, 425

electric organ evolved from, 293

functionless, 293, 306, 309, 412-413,
601, 606, 642

innervation of (see nerves)

not attached to eyeball, 606

oblique, function of, 303, 565

pathology of, 329, 331

primitive function of, 303, 546-565

reflexes of, 300-303

scleral thickness and, 415

space-perception and, 300-312

surgical interchange of, 311-312, 328-

taxonomically: [329

fishes in general, 303-305, 565

lampreys, 258-260, 556

elasmobranchs, 564, 642

sturgeons, 569

holosteans, 573-574

teleosts, 432, 578

anurans, 594

urodeles, 601

cscilians, 606

birds, 270, 642

monotremes, 665-666

marsupials, 671

placentals in general, 665-666

whales, 412-413

man, 36- 39, 37
orbicularis oculi, 39-40*, 41, 425, 445,

578, 644
platysma: thin, sheet-like muscles imme-
diately beneath the skin in mam-
mals— those which a horse uses to
'twitch off' a fly; vestigial in man
except on the head and neck; 389,
423
protractor lentis, 259-260, 262, 266-267,
269, 565, 567, 595, 597, 602, 608,

and ciliary folds, 372, 597 [610

pyramidalis

in chelonians, 42 1 -422

in crocodilians, 421

in birds, 420-421, 424
retraaor bulbi

derivative of (bursalis), 642

erroneous attribution to rays, 452, 692
(entry for p. 452)

history of, 419-420

leaving eyeball in adult, 606
taxonomically:

amphibians, 419, 421, 594, 601, 606
chelonians, 421-422, 427
crocodilians, 421-422
5pAenoc/on, 421, 617
lizards, 421

birds (lacking), 424-425, 642
monotremes, 665
marsupials, 671

placentals in general, 420, 427
sirenians, 408
whales, 412
man, 38
retractor lentis ('campanula Halleri'),

130-131, 261-262, 269, 567, 575,
577, 583, 605
striated, 269*, 630, 686-687
of temporary lids, 578
tensor chorioidea, 263*, 279, 577, 583-

584, 597, 605
transversalis, 269, 278-279, 299, 437,
608, 610, 614, 619, 624
musk-turtles: Kinostemidje, q.v.
Mustelidae (mammals: weasel family of
carnivores — mink, otter, marten,
amphibious, 443 [etc.)

optic axes in, 297
Mustelus (elasmobranch: a galeorhinid 'dog-
anterior segment of, 565 [fish')
area centralis of, 184-185, 187, 243, 245
lids of, 429

mydriatic pupil rigor in, 159
tapetum lucidum of, 243-245, 244
visual cells of, 184, 518, 561,568
mutations: unpredictable, marked, hereditary
peculiarities which appear in prog-
eny, but whose basis is in acciden-
tal changes in the germ-plasm of
the parental generation; e.g., the
occurrence of an albino in a nor-
mal strain or family
of loss, 389*
Muybridge, 352, 367

Mycteropercd (teleost: an epinephelid), eye-
movements, pupil, and possible
fovea of, 304-305
Myctophida (teleosts: a lantern-fish family)
habits of, 402
retina in, 399
stalk-eyed larva in, 405
Myctophum (teleost: a myctophid), onto-
genetic change of eye shape in, 405
Myliobatidae (elasmobranchs: eagle rays),

aim of eyes in, 386
Myliobatis (elasmobranch: eagle ray)
pelagic habit of, 243
pupillary operculum of, 386

760

INDEX AND GLOSSARY

Myliobatis — cont'd

tapetum lucidum (lacking) in, 243, 568
visual cells of, 243, 518, 561, 568
Myocastor: Myopotamus, q.v.
myoepithelial: said of epithelial cells which

are strongly contractile
myoid, 54*, 54-55
myopia, 27*, 27, 252-253, 547*

as normal for animals, 286
Myopotamus {-Myocastor; mammal: a

rodent; coypu), pupil of, 221
Mysticeti (mammals: baleen whales; see

whales)
Myxine (cyclostome: a hag) , eye of, 387, 562

N

Nagel, 490, 506

narwhal: Monodon; 412

nasad: toward the nose

nasad asymmetry, 173, 300*, 643, 678-679

carried to logical conclusion, 403
nasolacrimal duct (see lacrimal system)
Natrix (reptile: a colubrid snake)

amphibious species of, soft lens in, 438

dermal color changes in, 542

eye and accommodation in, 438, 456

scleral pigment in, 628

spectacle of, 456

development of, 454-455

visual cells of, 59, 63, 165, 637

visual fields of, 294
Nautilus (mollusc: chambered nautilus)

eye of, 3

development of, 119

pinhole pupil of, 256
Navy, U.S., color-filters of, 198
near point, 252-253*
near-sightedness: myopia, q.v.
neck, importance of , in vision, 303,305,307,
309,311,318,342,377,419,432
NectuTus (amphibian: a proteid urodele;
mud -puppy )

eye and adnexa of, 405-407, 601

lens index of, 602

retinal elements of
counts of, 603
size of, 603

scleral cartilages of, 602
needlefish: Belone, q.v.
Nematalosa (teleost: a clupeoid), adipose

lids of, 383
Nemestrinus (mammal: a macaque)

color vision in, 515

cerebral 'color cells' in, 523
Neobalccna (mammal: a baleen whale), 411
Neoceratodus (dipnoan: Australian lung-
fish), 136-137

eye size and habits of, 263

falciform process (?) in, 590

need for investigation of, 263, 589-590

optic nerve of, 591, 632

possible accommodation of, 263, 273

visual cells of, 591, 688
Neognathce higher birds), 650*; pecten in,

649-650
nerves associated with eye (see also optic
nerve)

vertebrates in general, 172, 422

taxonomically:

lampreys, 556

teleosts, 597

amphibians, 597

crocodilians, 422

Sphenodon, 617

lizards, 423

birds, 172

man, 38
neuroglia: ectodermal elements which serve
as the special conneaive tissue of
the central nervous system (see
also pecten, conus papillaris); 48-
49, 560, 569, 591, 631-632
neurohumors, 529*
neutral point, 98*, 470, 493, 516
Newton, 88

Newton-Miiller-Gudden, law of, 319-320*
newts (see Urodela)
Nicolai, 506
Nicolas, 156, 312

nictitans: nictitating membrane, q.v.
nictitating membrane, 118*, 420

consensual reflex of, 325

development of, 118

false, 383-384*

functions of, 420, 449, 452

lens-like action of, 273, 440

taxonomically:

elasmobranchs, 382, 429, 563

anurans, 266, 421,429, 593

urodeles, 601

chelonians, 42 1 -422

crocodilians, 421

Sphenodon, 421,617

lizards, 421,423,617

snakes, 455

birds, 118, 325, 420-421, 424-425
amphibious, 273, 440

mammals, 118, 412, 426-427, 443, 445,
665, 671
man, 38
night lizards: Xantusiidae, q.v.
night monkey: Aotus, q.v.
night-blindness: nyctalopia, q.v.
nighthawk, eyeshine of, 646
nightingale: Luscinia, q.v.
Noback, 665

INDEX AND GLOSSARY

761

Noble, 593, 599
nocmmality (see also habits)

adaptations for, 206-246, 410, 457-459,
563, 568, 613, 620-622, 624, 626-
627, 636-640, 661, 670-671, 674,
678, 684-689
paradoxical apparent (in seals) , 446-448
advantages of, 208-209
immateriality of emmetropia in, 288
limitations of, 208-209
ocular proportioning in, 173
pupil and, 217-228
retinal lamination and, 177
retinal metabolism and, 658
spectacle and, 457-459
nodding habit, 342
Nolte, 522

Nomarthra (order of mammals; 'edentates',
in part; pangolins; see Manis),
692 (entry for p. 676)
optic axes of, 297
pure-rod (?) retina in, 685
size of eye in, 677
taxonomic position of, 676
Notoryctes (mammal: marsupial 'golden
mole' )
eyes of, 210

scleral cartilages of, 671
Notropis (teleost: common shiner), color

vision in, 486
nurse shark: Gingylostoma, q.v.
nyctalopia: night-blindness; inability to see
in dim light (often mistakenly
called hemeralopia — which means
t/cjy-blindness); 77-78
Nycticebus (mammal: a lemuroid)
tubular eyes of, 677-678
visual cells of, 685
Nyctipithecus: Aotus, q.v.
nystagmus, 97*
caloric, 301*
railroad, 302*

occipital condyles: prominences on the base
of the skull, which articulate with
the first vertebra

occlusible, 237*

Ochotona (mammal: a lagomorph; pika),
diumality of, 201, 227, 686

octave: a span of frequencies or wavelengths
such that the highest is exartly
twice the lowest

oculorotatory muscles: those which turn the
eyeball, as apart from other extra-
ocular, oculomotor muscles such as
retractors, levators, nirtitans-oper-
ators, etc.; see muscles

O'Day, 227, 665-666, 669-670, 675
OdobcEnidae (mammals: walruses; see Pinni-

pedia)
Odontoceti (mammals: toothed whales; see

whales)
Oedipus (amphibian: a salamander), com-
plete terrestriality and viviparity
of, 368
Ogcocephalus (teleost: a batfish), stripes

crossing eye of, 546
Ogneff, 390, 533
oil-bird: Steatornis, q.v.
Onychodactylus (amphibian: an aquatic
salamander), flat cornea of, 601
operculum
of gills, 581

of pupil (see pupil, opercula of)
Ophidia: snakes, q.v.
Ophiops (reptile: a lacertid lizard), spec-
tacle of, 450
Ophisaurus (reptile: a legless anguid)
evolution of, 636
eyes of, 633
visual fields of, 294
ophthalmoliths, 239*
ophthalmoscope, 178, 185, 229*, 365

rhodopsin seen with, 231
opisthoglyphs : back-fanged colubrid snakes;

pupil in, 225
Opisthoproctus (deep-sea teleost), upward-
aimed tubular eyes of, 401, 403
opossums (mammals: lowest marsupials)
common: Didelphis, q.v.
cornea in, 671-672
development of, 663
elongated eye in, 671
eye size in, 674
eyeshine in, 238
intelligence (lacking) of, 467
lens shape in, 173, 213, 674
mouse: Marmosa, q.v.
optic axes of, 297
primitiveness of, 664
visual cells of, 215, 670, 675, 685, 688
Opsanus (teleost: toadfish), dorsal binocular

field of, 293
optic axis: a line through the centers of
curvature of the lens and cornea;
7, 291-297, 401-403
optic capsule, 557*
optic chiasma, 47, 52*, 319, 323, 334-335,

521, 666
optic cup, 104-109, 106

embryonic fissure of, 106, 118, 179, 265,
275, 277^278, 279, 437, 566-567,
575, 582, 597, 610, 650
healing of, 566-567, 582, 602
persistence of, 265, 562, 582

762

INDEX AND GLOSSARY

optic nerve (see also conus papillaris, pecten,
summation )
branching of, 367, 589, 606
chiasma of (see optic chiasma)
head of

blind spot created by, 1 78- 1 79
elongated, 179-180,576
eyeshine from, 230
multiple, 367, 589, 606
nerve-impulses in (see also retina, photo-
electric phenomena of), 80, 90-91,
103
proportion of decussation of, 319-320
taxonomically:
lampreys, 559-560
elasmobranchs, 569
sturgeon, 570
holosteans, 576
teleosts, 179, 261
cladistians, 589
dipnoans, 590, 632
cascilians, 606
crocodilians, 620
Sphenodon, 620
lizards, 632
snakes, 632, 635
birds, 643
mammals
monotremes, 666, 670
squirrels, 180, 367
whale, 413
seals, 445
man, 47, 51-52
optic pedicel, 564*, 564-565
optic radiations: the masses of geniculocor-
tical fibers— i.e., those which con-
nect the lateral geniculate bodies
with the visual cortex; 335, 337
optic tectum, 521*-522
optic tracts, 47, 52, 319*, 334-335, 521
optic vesicle, 105*, 105-106, 107-108
optical density, 22* -23

optomotor (optokinetic) reaction, 301*-302,
310
and study of vision, 492-493
Orbeli, 506, 692 (entry for p. 506)
orbit, taxonomically:
lampreys, 556-558, 557
elasmobranchs, 564-565
sturgeons, 569
teleosts, 578

electric organ in, 293
anurans, 594
CEecilians, 605
birds, 642, 650
man, 36, 39
Orcinus (mammal: killer whale), alleged
spying through air by, 411

Orectolobus (elasmobranch: a shark),

pupil of, 222
origin of eye, 119-133

orimentary: said of structures which seem to
have appeared in evolution before
there was any real use for them,
and which became useful only to
later, descendant, groups of animals
Ornithorhynchus (mammal: duck-bill;
habits of, 201, 443 [platypus)

ocular structure in, 664-671
pupil of, 221
relationships of, 138, 663
upward tilt of eyes in, 296
visual cells in, 59, 201, 670-671, 675
oil-droplets of, 692 (entry for p. 203)
Orycteropus (mammal: aard-vark)
ciliary body of, 679
cornea in

cornification of, 665
ovoid form of, 679
eyeshine and tapetum lucidum in, 241
nictitating membrane of, 426
optic axes of, 297 ('edentates')
pectinate ligament of, 680
size of eye in, 677
taxonomic prosition of, 676
Osawa, 617-619
Osbom, 530

osculant: said of a species or group related
to two others which it directly con-
nects— a living link as opposed to
a 'missing' {i.e., extinct) one
osmosis, 369-373*, 425, 529
Osphranter (mammal: a kangaroo), lens

size and shape in, 674
osprey, feeding method of, 439
ostrich: Struthio, q.v. (American: Rhea, q.v.)
Otaria (mammal: sea lion), eye of, 446
Otariidae (mammals: eared seals; see Pinni-
otter: Lutra, q.v. [pedia)

Ouradnik, 551
Ovio, 322, 350
owl parrot: Strigops, q.v.
owls

accommodation in, 281, 655
ancestry of, 190, 208
area temporalis and fovea of, 187-188,
308-309
elongated visual cells of, 692 (entry for

p. 195)
as pupillomotor area, 185
'blindness' in daytime of, 168
cornea : retina areal ratio of, 289
critical fusion frequency of, 354
eyes in

closure of, as habit, 546-547
frontality of, 309, 320,331,413

INDEX AND GLOSSARY

763

immobility of, 213, 309, 329, 413, 642

size of, 642-643

tubular form of, 212-213, 642-643
eyeshine in, 240, 646
hiding posture of, 546
iris in

coloration of 545-546, 548, 550-551

rupture of, 647
lacrimal system of, 425
lids, white, in, 546
nictitating membrane in

cloudiness of, 424

tendon pulley of, 425
oculorotatory muscles of, 213, 642
optic chiasma of, 320, 329
orbit of, 424
pecten in, 643, 655-656

shadows of, 365
photopic spectrum of, 500-502
pupils of, 226, 501-502
retina in, 661

angular size of, 289, 642, 656

summation of, 661
rotatability of head in, 213, 309
scleral ossicles of, 644
scotopic spectrum of, 102, 500-502
tapetum lucidum (claimed for), 646
visibility of infra-red to, 502
visual capacities of, 206, 216, 323-324,

366, 500-502
visual cells in, 215-216, 500, 661

foveal, 692 (entry for p. 195)

oil-droplets of, 201

rhodopsin of, 157
visual fields of, 289, 295, 308-309
ox: Bos, q.v.

Oxybelis (reptile: a colubrid tree-snake),
eye-mask of, 545

paddlefishes : Polyodon, Psephurus, qq.v.
Pagellus (teleost), development of sclera in,
painted turtle: Chrysemys, q.v. [579

painting

depth in, 194

illuminatioix of, 199
palm civet: Paradoxurus, q.v.
palpebral fissure (see lids, aperture of)
Palaeognathas (lower birds), 650*; pecten in,

648-650, 649, 656-657
Palmer, 603

panda, giant, nictitating membrane of, 427
pangolins: Manis et al; Nomarthra, qq.v.
Pantodon (teleost: butterfly-fish), amphib-
ious behavior of, 431
papillose: beset with papillee
Papio (mammal: Guinea baboon), color
vision of, 515

Paradoxurus (mammal: a viverrid carnivore;
palm civet), horizontal slit-and-pin-
hole pupil of, 221, 227-228, 256
parakeet (see Melopsittacus)
Paralichthys (teleost: a flounder), dermal

color changes of, 482
parallax, 314*-315, 342, 348, 361
paranuclear body, 59, 61*, 692 (entry for p.
parapineal eye (see median eyes) [59)

parasite: an organism which lives at the
expense of, and does harm to,
another organism of a different
species (c/. commensal)
parasitic fishes, 209-210, 387, 390-391
parietal eye (see median eyes)
Parinaud, 64
Parker, 535-537
parrots

color vision of (see Melopsittacus)
fixation by, 307
habits of, 657
lower lid of, 424
oil-droplet colors of, 502-503, 657
pecten in, 657
visual fields of, 295, 657
pars CcBca retinee: the thin, blind, anterior
continuation of the retina, extend-
ing from ora terminalis to pupil
pars ciliaris retinae: the jwrtion of the pars
CcBca which covers the inner surface
of the ciliary body
pars iridica retina: the portion of the pars
caeca which covers the posterior
surface of the iris
pars optica retina: the seeing portion of the
retina (i.e., the portion provided
with visual cells), posterior to the
ora terminalis
pars plana: the flat portion of the ciliary

body; orbiculus ciliaris
pars plicata: the anterior portion of the cil-
iary body, which bears the ciliary
processes; corona ciliaris
Parus (bird: titmouse), perten shadows of,
Passer (bird: English 'sparrow') [365

canal of Schlemm in, 646
eyes and brain of, 172
foveal-cone concentration of, 661
pecten shadows of, 365
retina of, 659, 661
visual cells of, 660-661
Passeri formes (perching-bird order)
area and fovea in, 187
laterality of eyes in, 295
oil-droplet colors in, 197, 502
pecten in, 655
scleral ossicles in, 274
visual capacities of, 655

764

INDEX AND GLOSSARY

passerine birds: Passeriformes, q.v.
Patella (mollusc: limpet), eye of, 3
Pauli, 538
Pavlov, 507

pearl-fish: Encheliophis, q.v.
pearls, artificial, 235

pecten (see also conus papillaris), 118, 180,
188, 308, 365-367, 625, 643, 649

significance of, 648-659

size of, 655-657
Pedetes (mammal: a rodent, not a lago-
morph; Cape jumping 'hare' ) , pin-
hole pupil of, 162, 221, 228, 257
Pegel, 491
Pelagosaurus (reptile: extinct crocodilian),

scleral ossicles of, 274
Pelecus (telecst: a cyprinid), retinal tapetum
pelicans [lucidum of, 236

eye mobility in, 307

feeding method of, 439
Pelobates (amphibian: an anuran)

pupil of, 223

scleral cartilage of, 595
Pelobatidce (amphibians: an anuran family),
oil-droplets (lacking) in, 599-600
penguins

binocular vision in, 291, 295

depth of diving by, 226

feeding habits of, 439-440

lacrimal system of, 425

orbit of, 307

pupilsof, 221,226, 439

reaction to movement by, 344

seasonal changes of iris color in, 550

taxonomic position of, 650

vision of, 273, 344, 439, 448
Perameles (mammal: a bandicoot), conus

papillaris of, 672
Perca (teleost: perch), visual-cell mosaic of,
Percidae (teleosts: perch family) [587

binocular field in, 292

horizontal cells in, 585

retinal tapetum lucidum in, 236-237, 240,
percoids: Percidae et al [585

optic nerve and disc in, 179

spertacles in, 460
perimeter: a clinical instrument for mapping

the visual field of the eye
Periophthalmus (teleost: mud-skipper), 431

annular ligament of, 581

eye and habits of, 43 1 -43 3

flatness index of lens in, 435

sphincter pupillee of, 160
periscopy, 214, 291, 297, 376-377*, 414

agility as substitute for, 445 (c/. 444,

horizontal pupil and, 293, 443 [bottom)
Perissodactyla (mammals: odd-toed 'ungu-

avascular retinze of, 684 [lates'), 676*

ciliary processes of, 681

cones of, 688

corpora nigra of, 679
Perlia, nucleus of, 302*

Perodicticus (mammal: a lemuroid), color
vision and cerebral 'color cells'
(lacking) in, 523
persistence-time (see retinal image)
perspective, 314*

aerial, 314*
Petaurus (mammal: a flying phalanger;
marsupial 'flying-squirrel'), 664

possible tapetum lucidum of, 241, 672
Peters, 404

Petit, canal of, 7, 19*
Petit, 692 (entry for p. 409)
petrels, feeding method of, 439
Petromyzon (cyclostome: a lamprey)

chorioid of, 558

size of eye in, 556

visual cells of, 560-561
Petromyzonida (cyclostomes: northern lam-
prey family), 555*, 562
Phalacrocorax (bird: cormorant)

accommodation in, 273, 440-441

anterior segment of, 441

coloration of eye and vicinity in, 547-548

depth of swimming in, 226

and guano, 235

habits and eye of, 439-441

orbit of, 307

ringwulst of, 647
phalangers: an assemblage of marsupial

ecology of, 664 [mammals

flying-: Petaurus {q.v.), et al; 664
Pheophilaktova, 506
Phelsuma (reptile: a lidded gecko)

diurnality of, 203, 465, 627

possible color vision of, 465, 520

pupil of, 203, 220, 627

visual cells of, 203, 520, 627
phi-phenomenon (see movement, strobo-

scopic apparent)
Phoca (mammal: a seal)

diagonal slit pupil in, 221, 228, 448

ocular structure and vision in, 445-448,

optic axes of, 297 [446

tapetum lucidum in, 234
Phoccena (mammal: porpoise), eye of, 413
Phocidae (mammals: true seals; see Pinni-
P holts (teleost), fovea in, 304 [pedia)

Photoblepharon (teleost), photophore associ-
ated with eye in, 396-397, 405
photochemical substances in vision (see also
iodopsin, porphyropsin, rhodopsin,
zapfensubstanz), 464
photochromatic interval, 92*
photocyte, 53*

INDEX AND GLOSSARY

765

photophobia, 97*

photophores, 396*-397, 398, 401-403, 404

Phoxinus (teleost: Ellritz)

color vision in, 479-480, 487-488, 492, 522

color-associations and brain surgery in, 522

dermal color changes in, 480-482
diurnal rhythm of, 538

retinal photomechanical changes in, 146,

stroboscopic vision of, 363-364 [480

Phrynomerus (amphibian: an anuran),

pupil of, 223
Phrynosoma (reptile: an iguanid lizard),

dermal color changes in, 540
Phyllorhynchus (reptile: a colubrid snake)

fibrous tunic of, 628

speaacle of, 450

visual cells of, 168, 216, 638
rhodopsin (lacking) in, 78, 168
phylogeny (see evolution)
Physeter (mammal: sperm whale)

habits of, 411-412

visual cells of, 415
Physignathus (an agamid lizard), visual

fields of, 294
Physoclisti (a teleost division)

characteristics of, 576-578

double (?) cones in, 587

falciform process in, 582
Physostomi (a teleost division)

chararteristics of, 576-578

cornea in, 579

falciform process in, 582

horizontal cells in, 585
pia-arachnoid (see meninges)
Piabuca (teleost), vertical pupil of, 220, 222
pig (see Suina)

pigeon, domestic: Columba, q.v.
pigeon guillemot: Cepphus, q.v.
pigment (see also carotenoids, chlorophyll,
melanin)

chorioidal, funaion of, 13, 228

of cornea, 219

of lens (see also lentiflavin), 199

at limbus in reptiles, 609

of macula lutea, 204

migration of

in retina, 146-152
in skin, 525-526

photochemical (see idopsin, porphyropsin,
rhodopsin, zapfensubstanz )

photosynthetic, 374

of retina (see retina, pigment epithelium
of; fuscin)
pika: Ochotona, q.v.
pikeperch: Stizosledion, q.v.

European: Lucioperca, q.v.
pineal eye (see median eyes)
pineal gland, 339*

pinhole

as image-former, 2, 224, 255-257
-pupil,220-223, 224-225, 227-228, 391
relation to accommodation of, 255-257,

438
simulation of, in seals, 447-448
Pinnipedia (mammals: eared and true seals,
walrusses)
accommodation and refraaion in, 272-273,
ciliary processes in, 681 [447-448

eyes, vision, habits of, 443-448, 446
iris of, 678
lens in, 683

muscle of Miiller in, 285
optic axes in, 296-297
pectinate ligament of, 680
pupils in, 162-163, 221
retina in, 216

tapetum lucidum of, 233-235, 241, 244
taxonomic position of, 139, 676
upward tilt of eyes in, 296
Pipa (amphibian: Surinam toad), aquatic

habit of, 368
pipe-fish: Syngnathus, q.v.
Piper, 500-501

PipidcP (amphibians: an anuran family)
pupils in, 223
spectacle in, 593
Pipistrellus (mammal: a microchiropteran),

retinal capillaries in, 684
Pirenne, 502
Pisa, 292, 298

Pithecus {-Macacus [in part]; mammal:
Sumatran monkey), color vision
pit-vipers: Crotalidas, q.v. [of, 515

placental mammals (see also human eye
and vision)
accommodation and refraaion in, 252,
257, 272-273, 283-288, 444-448,
adnexa in, 425-427 [680-683

amphibious, and their adaptations, 442-448
aquatic, and their adaptations, 407-417
area centralis and fovea in, 181-182, 187,

190, 245, 292, 311-312
arhythmic, 145

central visual pathway in, 335
chonoid in, 254-255, 672, 678
ciliary body in, 286, 679-683

muscles of, 272-273, 285-286, 674
color vision in, 333-338, 462-472, 504-

523, 688-689
coloration of body and eye in, 523-524,
compared with snakes, 687 [543-550

conus papillaris in, 654
development of eye in, 104-117
diurnal, 686, 692 (entry for p. 201)
early ocular history of, 283-284, 686-689
eye-movements of, 310-312, 330

766

INDEX AND GLOSSARY

placental mammals — cont'd
eyes of, 676-689

habits of, 143, 145, 169-171, 176-178,
201, 203-204, 208-210, 227-228,
296, 310-312, 677, 684-689
imitation of, by marsupials, 664
intraocular color-filters of, 143, 191, 199,
ins in, 648, 679 [201, 204-205

lens in, 674, 680-684

yellow coloration of, 143, 199, 201,
204-205
movement-perception of, 342-365
nasad asymmetry in, 173, 300
ocular proportions in, 171-175, 173, 211-
214, 213, 255, 300, 672, 677-678
optic axes in, 296-297
optic chiasma in, 52, 319-320, 330
optic disc in, 179-180

multiple, 367
origin and evolution of, 134-135, 138-139,

284, 675-676, 686-689
pineal gland (epiphysis) of, 339
pupils of, 150, 154-158, 162-163, 218-
219, 221, 227-228, 245, 256-257,
corpora nigra of, 219 [299

retina in, 49-50, 176-178, 187, 217,
684-689
circulation of, 50-51, 191, 201, 204,
654, 684
sclera in, 678
tapetum lucidum and eyeshine in, 232-233,

228-235, 238-239, 241, 243-246
vision of, 145, 168, 211-212, 215-216,

245-246, 338
visual acuity in, 207, 245-246
visual cells of, 56-58, 166, 176-178, 201,

215-217, 245, 588, 684-689
visual fields of, 289-292, 296-298
Platanista (mammal: a blind dolphin; susa),
habitat and degenerate eye of, 210,
Plateau, 357 [412

Plath, 499-500
Platichthys (teleost: a flounder), pupillary

operculum in, 386
platinic chloride, as test for rhodopsin, 75
platypus: Ornithorhynchus, q.v.
Platyrrhina (mammals: New-World anthro-
poids), taxonomy and color vision
of, 516-517, 521
platysma (see muscles)
Platytroctes (deep-sea teleost), shape of eye

in, 402
Plecostomus (teleost: an armored catfish),

operculate pupil of, 158, 222, 386
plectognaths (teleosts), 580*
corneal laminations in, 580*
falciform process (lacking) in, 582
vitreal vessels in, 582-583

Plethodon (amphibian: slimy salamander),

retinal summation of, 603
PlethodontidsE (amphibians: a urodele fam-
sclera in, 601 [ily)

taxonomic position of, 600
PleuTonectes (teleost: a flounder), dermal

color changes in, 534
Pleuronectidae (teleosts: right-handed floun-
ders), turreted eyes and pupils of,
386
PleuTOsauTus (reptile: extinct rhynchoceph-

alian), scleral ossicles (lacking)
plica semilunaris, 38* [in, 274

plumula Halleria: campanula, q.v.
Podargus (bird: frogmouth)

adaptation for bright retinal image in, 642
crepuscularity of, 208
eye-closing habit in, 546-547
eyeshine in, 240
feeding method of, 169
as owl ancestor, 309
pecten of, 656
scleral ossicles of, 644
tubular eye of, 212, 642
P6tzl, 364

poikilochromic: capable of changing color
poikilothermous : said of so-called cold-blood-
ed animals — i.e., those whose body
temperature is not under physiol-
ogical control and hence approxi-
mates that of the environment
polar bear (see bears)
polecat: Putorius, q.v.

Polistotrema (cyclostome: a hag), eye of,
Pollachius (teleost: pollack) [562

falciform process in, 582
visual cells of, 586
pollack: Pollachius, q.v.
Polydactylus (teleost: a polynemid), cornea

and spectacle in, 450, 460
Polyipnus (deep-sea teleost), branched optic

nerve of, 367
PolynemidsE (teleosts: a percoid family),

spectacles in, 460
Polyodon (chondrostean: spoonbill), 137,

264, 569; binocular vision in, 292
Polypedates (amphibian: Javanese flying-
frog), pupil of, 223
Polypedatida (amphibians: an anuran fam-
oil-droplets (lacking) in, 599-600 [ily)
pupils of, 223-224
Polyprion (teleost: a serranid), guanin in

retina of, 585
Polypterus (cladistian: bircher)
eye of, 263, 589

eyeshine and tapetum lucidum in, 240
habitat of, 136, 588
multiple optic papilla of, 367, 589, 606

INDEX AND GLOSSARY

taxonotnic position of, 136

visual and horizontal cells of, 692 (entry
for p. 589

vitreal vessels of, 605, 653
Pomolobus (teleost: a clupeid; skipjack),

adipose lids of, 383
porbeagle shark: Lamna, q.v.
porcupines (mammals: rodents)

New-World: Erethizontidcc; color blind-
ness of, 513

Old-World: Hystricidae, q.v.
porphyropsin, 375*
porpoise (see whales)
Porsch, 503-504
Porter (see Ferry and Porter)
Portier, 310

potto: Perodicticus, q.v.
Pouchet, 479, 529

Pouchetia (protozoan), visual organelle of, 3
Poulton, 524

prsBSCopic larvce, 401, 405*
prairie-dog: Cynomys, q.v.
pre-adaptation, 388*, 399
predacity, visual fields and, 290-291
presbyopia, 35-36*, 250, 257, 285, 440

freedom (?) of non-mammals from, 287
pressure, hydrostatic

intra-ocular, 12*, 275, 279, 417

ocular adaptations to, 394-395, 415-417
Primates (order of mammals: Lemuroidea +
Anthropoidea, qq. v.); see also
human eye and vision

accommodation and refraction in, 272-
273, 287, 681-683, 689

area centralis and fovea in, 187, 190, 245,
685, 689
macula lutea, 181, 201, 204

central visual pathways in, 334-338, 335

ciliary muscles of, 285, 679
of Miiller, 280, 285

ciliary processes of, 681-683

circumcorneal sulcus of, 284, 672

color vision in, 515-517, 519-523

compared with monotremes, 669

convergence in, 312

evolution of diurnality in, 515, 521, 688-

eye-movements in, 311 [689

flexibility of neck in, 213, 311

habits of, 169, 176, 201, 204, 227-228,
286, 504

intra-ocular proportions in, 174

iris in, 678

coloration of, 545, 550, 679

lens in, 201, 683

need for binocularity in, 312

nictitating membrane in, 426

optic axes in, 297

optic chiasma in, 319-320

origin and evolution of, 135, 139, 504,

516-517, 676
pupils of, 221, 227-228
retina in, 201, 685-686

vessels of, 654, 684
size of, 228

size of eye and image in, 176, 677
surgical interchange of eye muscles in, 312
tapetum lucidum in, 233, 241, 245
visual cells of, 685-686
visual fields of, 296-297
zonule in, 682-683
Prionace (elasmobranch: great blue shark)
habits and nictitating membrane of, 429
pupil of, 220, 222
Pristis (elasmobranch: sawfish)
entering fresh water, 372
habitus and ocular aim of, 385
Pristurus (reptile: a diurnal gecko), pupil

and visual cells of, 627
Proboscidea: elephants, q.v.
Procavia (mammal: hyrax; cony)
cones of, 688
diurnality of, 686

pupil and umbraculum of, 219, 221-222
taxonomic position of, 676
Procoela (amphibians: an anuran suborder),
Proechidna: Zaglossus, q.v. [593

PromicTOps (teleost: an epinephelid; spotted
jewfish), eye-movements, pupil,
and possible fovea of, 304-305
pronghorn: Antilocapra, q.v.
Propithecus (mammal: an indrisine lemur),

diurnality in, 515
ProsimicB: Lemuroidea, q.v.; 228*, 515*
protanopia, 99*
protective devices (see adnexa, coloration,

spectacle)
ProteidcE (amphibians: a urodele family;
Necturus + Proteus [ + Haideo-
triton?])
ocular and other characteristics of, 600
scleral cartilages in, 602
Proteus (amphibian: European cave sala-
mander; Grottenqllm)
degenerate eye of, 390, 407

recrudescence of, 390
scleral cartilages of, 602
Protopterus (dipnoan: African lungfish)
accommodation (lacking) in, 263
chorioid of, 590, 654
compared with lamprey and amphibian,
cornea of, 590 [604-605

dermal color changes in, 537
habits of, 222-223
iris of, 220, 222, 590
lens of, 590
optic nerve of, 591

768

INDEX AND GLOSSARY

Protopterus — cont'd

pupil of, 160, 220, 222, 590
relationships of, 135-136, 589
retina of, 263, 590-591, 598
pigment epithelium of, 44
sclera of, 590
spectacle of, 590

visual cells of, 55, 591, 600, 605
vitreal vessels of, 590, 653-654
Psammophis (reptile: Saharan arrow snake),

spectacle of, 450
Psephurus (chondrostean: a spoonbill), 137,

264, 569
Psettodes (teleost: primitive flatfish), migra-
tion of eye in, 385
Pseud acris (amphibian: a hylid anuran),
scleral cartilage (lacking) in,
595, 602
Pseudemys (reptile: a terrapin), nocturnality

and rod: cone ratio of, 216
pseudo-tapetum : retinal tapetum lucidum;

235*
pseudobranch, 118, 581*, 598
Pseudopleuronectes (teleost: winter floun-
der), dermal color changes in, 530
Pterois (teleost: lionfish), concealing color-
ation of eye in, 546-547
Pteromys (mammal: giant flying-squirrel;

taguan), possible tapetum lucidum
Pteropus (mammal: a fruit-bat) [in, 241

retina and chorioid of, 255
retinal tapetum lucidum of, 684
puffers: Spharoides (q.y.) et al
falciform process (lacking) in, 582
peculiar corneae of, 580
vitreal vessels of, 582-583
punctce lacrimalia, 39-40*
pupil (see also iris, muscles of; pinhole)
accommodation and, 272-273 (Table
amuscular, 160, 222-223, 590 [VIII)
aphakic space of, 185-186, 221, 261, 293
fovea and, 185-186, 305
visual field and, 290, 299
blocking of, by lens, 264, 376, 434, 437-

438, 440-441, 444, 592
changes of, 76-77, 80, 150 (Table II),
153-163, 679
reflex, 156-158, 185, 325, 475, 630
speed of, 157, 222, 501, 614
concealment of, 544, 548-549
control of, 185, 475

voluntary (?), 156, 162, 446
corpora nigra of, 2 1 9, 679
in deep-sea fishes, 398-400
double

apparent, 433-434
real, 434-435, frontispiece
effect of wavelength on, 474, 500-501

functions of, 17-18, 153-154, 214, 428, 630
keyhole, 185-186; 221, 225, 293, 299.
lid-opening and, 428, 447, 630
mydriatic rigor of, 159*, 159
nodules of, 266-267, 596-598, 692

(entries for pp. 266, 273 )
operculum of, 158-160, 219-222, 228,
dual, 222 [386, 414

umbraculum type of, 219
response to drugs by, 157
sexual differences in, 226
shapes of, 217-228, 218-219, 223, 225,
678
distribution of, 220-221 (Table VI)
size of

efl^ects of, 211-212, 214, 225, 377, 386
physiological, 77, 156-157
in sleep, 630

slit, 165-168, 203, 223-224, 627
lid-opening and, 428, 447
orientation of, 428, 447
rarity of, in birds, 226
visual field and, 225, 293, 299, 376, 443,

447, 592-593
TAXONOMiCALLY, 220-221 (Table VI)

and:
lampreys, 158
elasmobranchs, 150, 155, 158-159, 219,

222, 224-225, 382
sturgeons, 160, 222
holosteans, 222
teleosts, 158, 160-161, 222, 382-383,

433-434, 435, frontispiece
dipnoans, 150, 160, 222-223, 590
amphibians, 157-158, 161, 218-219, 223-
224, 592-593, 596, 692 (entries
for pp. 266, 273 )
chelonians, 224, 437
crocadilians, 224, 501
Sphenodon, 224
lizards, 224

geckoes, 166, 168, 203, 223-224, 627
snakes, 166, 221, 225
birds, 162, 226, 439, 501
monotremes, 668
sirenians, 410
whales, 414

man, 17-18, 68, 76-77, 80
pupillary membrane, I 15-116*
pupilloscopy, pupillometry: measurement of
the pupil as a criterion of bright-
ness; 475, 491
Purkinje phenomenon, 87-88*, 92, 491*
isochromatic, 475*

TAXONOMICALLY:

fishes, 474-475, 477-478, 486, 490
amphibians, 490-491, 493
crocodilians, 496

INDEX AND GLOSSARY

769

birds, 500-501

mammals, 509-511
Putorius (mammal: a mustelid carnivore;

polecat), sensory capacities of, 508
Pygopodidae (reptiles: snake-lizard family)

contrasted with snakes, 634, 636

habits of, 200

loss of fovea by, 621, 625

pupils of, 220

spectacles of, 450

visual cells of, 200, 626
Pygopus (reptile: leaf- footed lizard)

conus papillaris of, 653

evolution of, 636
pyriform : pear-shaped
Python (reptile: a pythonine boid snake)

canal of Schlemm in, 629-630

ciliary body of, 629

hyaloid vein of, 629

optic axes of, 294

retina of, 636

scleral pigment of, 628
pythons: Pythoninas (a boid sub-family)

rabbits (and hares)

ciliary muscle of, 286

color change in, 524

color vision in, 511-512, 521

electroretinography of, 521

eye-movements of, 310, 312

fixation by, 310

laterality of, 291, 296
optic axes and, 297

lid-reflex, non-consensual, of, 425

optic chiasma in, 320

speed -sense of, 345

visual fields of, 296-298
Rabl, 655

raccoon, color vision in, 507-508
racers: Coluber and related genera

iris 'C ^f, 549

yellow lenses of, 199
Radford, 198
Rahn, 542
rainbow snakes: the colubrids Abastor and

Farancia, qq.v.
Raja (elasmobranch: a ray), 692 (entry for
p. 386)

eye of, 158, 255

retraaibility of, 429

operculate pupil in, 158, 222

stenopaic aaion of, 224-225, 256, 386

range of, 394

retina in, 568

ramp arrangement of, 255

toleration of light by, 429
Ramon y Cajal, 322

Rana (amphibian: common frog: see also

color vision in, 491-494 [Anura)

cornea of, 601

dermal color changes of, 535-537

eye of, 594-595

eye-mask in, 545

iris folds of, 596

pupillary nodules of, 595-596

retina in, 148

photomechanical changes of, 148

scleral cartilage of, 595

scotopic spectrum of, 101

visual cells of, 54-55, 59, 148, 599
rhodopsin in, 101
Ranidae (amphibians: common frog family)

habits of, 436

taxonomic position of, 593

visual cells in, 598-599
rapid peering, 341*

Rastrelliger (teleost: a scombrid), adipose
rat: Rattus sp. [lids of, 383

color vision in, 508-510

eye-movements of, 312

optic axes of, 297

optic chiasma of, 319

vision of, without cortex, 337

visual acuity of, 207, 312, 353

visual cells of, 215-217
Ratites (ostrich-like birds), binocular fields

of, 295
rat's-tails: Coryphasnoididas, q.v.
rattlesnakes: Crotalus {q.v.) , Sistrurus
Rayleigh effect, 197*
rays: Batoidei (in part), q.v.
Redfield, 540
Reeves, 481, 483-487, 489
reflection coefficient, 244* (see also albedo)
refraaion (see also accommodation, dioptrics)

of eye: the condition (or the determin-
ation of the condition) of an eye
with regard to astigmatism, hyper-
metropia, myopia, etc.; 272-273
(Table VIII), 286-287

TAXONOMICALLY:

lampreys, 258
elasmobranchs, 260
teleosts in general, 263
Periophthalmus, ^llA^i
Anabas, 431
amphibians, 436
chelonians, 436-438
crocodilians, 436
birds, 439-442

mammals in general, 444, 669
sirenians, 409
seals, 447-448
of light, 22*, 22-23, 24

index of, 22*, 29, 183-184, 265, 436

770

INDEX AND GLOSSARY

refraaive errors: astigmatism, hypermetropia,
myopia, qq.y.
amphibious vision and, 430, 669
of seals, meaning of, 447-448
Reighard, 473, 476, 484
reindeer

lid movements of, 425
nictitating membrane of, 427
relief, perception of (= stereopsis, q.v.),

idea vs measurement of, 315
reniform : kidney-shaped
reptate: to creep or crawl without benefit of
legs, or with the belly in contact
with the substrate
Reptilia, 134, 138, 607-640 (see sub-indices
on pp. 607, 608, 613, 616, 622)
general ocular pattern of, 607-608, 671
comparison with mammals, 663, 666,
669, 671, 674-675, 680-681, 686
departures from, 622
perpetuated in birds, 622, 641
perpetuated in mammals, 686
visual fields in, 294 (Table IX)
resolution, resolving power (see visual acuity)
rete mirabile, 574*

retina (see also area centralis, fovea, sum-
mation, pars, visual cells)
A and B (of lampreys), 117-118
accessory, of tubular eye, 257, 400-401
acidulation of, 102
amacrine cells of, 43, 49*, 660
ancestry of, 128-129

bipolar cells of, 43, 46* (and see sum-
mation)
circles of innervation in, 350*
circulation of, 204, 231, 262, 406, 410,
654, 670, 672, 684 (and consult
648-659)
in area centralis, 182, 204, 654
development of, 112-113
conneaions to brain of, 319-338, 335
corresponding points of, 317*-318, 322,
degeneration of, 228 [329-331

detachment of, 646
development of, 107-109, 560
in diurnal animals, 175-178, 177
external limiting membrane of, 43-44, 45*
ganglion cells of, 43, 47*-48 (and see

summation)
horizontal cells of, 43, 49*
inner nuclear layer of, 43, 46-47

lack of, 572
invisible raphe of, 319
laminal purity of, 585*
taxohomically:
teleosts, 585
chelonians, 611-612
lizards, 625

birds, 625, 659-660, 684

mammals, 43, 684-685
Mailer fibers of, 43, 48*, 572, 603, 620,
nerve-fiber layer of, 43 [660

medullated band in, 684
neuroglia of, 48-49
in nocturnal animals, 177, 215-217
nutrition of, 50-51, 583, 603, 615, 625,

635, 648-659, 672
outer nuclear layer of, 43, 46*
periphery vs center of, 352-356
photo-electric phenomena of, 78-79, 101,

489-492, 500, 521
photomechanical changes of, 145-163,
146-148, 166, 238, 265, 437,
585, 606, 626

acid and, 151

adrenalin and, 151, 478

distribution of, 150 (Table II)

wavelength and, 480
pigment epithelium of, 42, 43-44

oil-droplets in, 572-573

unusual pigmentations of, 228, 244,
478, 568, 572, 659, 672, 684
plexiform layers of, 43, 47*, 660
polarization of, 531-532
pure-rod, 216
pupillomotor area of, 185
ramp arrangement of, 255
refractive index of, 183-184
regeneration of, 109, 692 (entry for p.
thickness of, 585 [109)

taxonomically:
lampreys, 117-118, 177, 184, 518,

559-562
elasmobranchs, 568, 692 (entry for p.
568)

deep-sea, 399-400, 568
sturgeons, 242, 572
holosteans, 576
teleosts, 433-435, 583-588, 659

deep-sea, 257, 396, 399-400, 401

eels, life-cycle and, 405-407
cladistians, 589, 692 (entry for p. 589)
dipnoans, 590-591

amphibians, 148, 161, 598-600, 603, 606
chelonians, 161, 437, 611-612
crocodilians, 162, 615-616
Sphenodon, 189, 620-621
lizards, 161-162, 611, 620-621, 625-627
snakes, 166, 634-640, 636, 638
birds, 162, 646, 659-662, 660
monotremes, 669-671
marsupials, 672, 674-675
placentals, 684-689

sirenians, 409-410

seals, 446-448

man, 43-44, 684, 689

INDEX AND GLOSSARY

771

retinal image

barrel distortion of, 354

enlargement of, 66

by foveal clivus, 183-184

by optical employment of cornea, 417

as formed by pinholes, 224

'growth' of, 344

illumination of, 211-212, 224, 245, 448,

keystoning of, 317 [652

motion of, 347-352

peripheral vs central, 352-356

persistence-time of, 349-365, 350*
and grades of movement, 351

size of, 66, 171-175, 210-212, 245, 620,
retinal rivalry, 3 1 6* , 3 3 2-3 3 3 [642

Revesz, 499
Reynolds, 509
Rhamdid (teleost: a cave catfish), retention

of good eyes by, 387, 390
Rhea (bird: American 'ostrich')

pecten of, 649, 656

ringwulst of, 648
rhesus monkey: a macaque, q.v.

color vision of, 515

visual acuity of, 207
Rhineodon (elasmobranch: whale shark),

thick sclera of, 569
Rhinoceros

avascular retina of, 51, 201

false blink of, 427

nictitating membrane of, 426

taxonomic position of, 676

weak tapetum lucidum of, 241
Rhinocheilus (reptile: a colubrid snake)

basis of sensitivity in, 168

visual cells of, 63, 168, 638
Rhinophis (reptile: a uropeltid snake)

apertured spectacle of young, 455

glandular adnexa in, 424
Rhodophyceae (red algce), photochemical

adaptation to deep water in, 374
rhodopsin, 74-76*

absorption spectrum of, 101, 373-375, 462

derivatives of, 464

direct observation of, 103

distribution of, 691 (Plate I)

invention of
original, 163
other, 63, 165, 168, 375, 465, 518

in nocturnal forms, 206

ophthalmoscopic visibility of, 231

properties of, 53, 74-79, 462

relation of

to pupil, 155, 157

to scotopic brightness, 92, 101

role of, in dark-adaptation, 76-80, 155

sensitivity and, 70-71

solvents and tests for, 75, 100

TAXONOMICALLY:

lampreys, 562
chelonians, 611-612
crocodilians, 611, 616
geckoes, 63
snakes, 636, 638

absence from double rods of, 63
birds, 661
Rhomboidichthys (teleost: a pleuronectid ) ,

dermal color changes of, 482
Rhombus (teleost: a pleuronectid), dermal

color changes of, 482
Rhynchocephalia (order of reptiles; see

Sphenodon, Pteurosaurus) , 135,
rhythms, diurnal, 538 [ 138, 622

Riley, 499

river snakes: Homalopsinse, q.v.
robin: Turdus, q.v.

Rochon-Duvigneaud, 216, 246, 292, 306-
307, 312, 661, 692 (entries for
pp. 568, 589
Rodentia (order of mammals)
aquatic, 443
area centralis in, 187
ciliary processes in, 681
color vision in, 508-515
conus papillaris in, 654
eyes of, 680

size of, 677
eyeshine and tapetum lucidum in, 230, 241
habits of, 170, 201, 209, 443, 508, 692
lens in [ (entry for p. 201 )

coloration of, 201
shape of, 213, 683-684
niaitating membrane in, 426
ocular glands of, 426
optic axes of, 297
pupils of, 221, 227
retinal circulation in, 201, 684
taxonomic position of, 139, 676
visual cells of, 216, 685
visual fields of, 296-297, 310
Rotscheu, 476*
Roth, 510
rugose: set with ridges or with wrinkles

which cannot be 'smoothed out'
Rutilus (teleost: a cyprinid)
double (?) cones of, 586
retinal tapetum lucidum of, 586, 692
(entry for p. 236)
Rynchops (bird: black skimmer), 692 (en-
try for p. 221); unique slit pupil
of, 221, 226

saccadic eye-movements (see eye-movements)
Saccopharynx (deep-sea teleost), vestigial
Sachs, E., 100, 348 [eye of, 398

772

INDEX AND GLOSSARY

Sachs, M., 500

Sackett, 513

Saimiri (mammal: squirrel monkey), color

vision of, 515, 517
salamanders: Urodela, q.v.
Salamandra (amphibian: a salamandrid

aerial emmetropia of, 268 [urodele)

green rods (lacking) in, 603

rhythmic dermal color changes in, 538
SalamandridcB (amphibians: a urodele

sclera in, 601 [family)

taxonomic position of, 600
Salmo (teleost: some trouts, Atlantic salmon)

adipose lids in, 383

development of sclera in, 579

double (?) cones in, 586

visual-cell mosaic in, 587
Salmonids (teleosts: salmons, trouts, etc.)

binocularity and frontality in, 292

color vision in, 466-467

dermal color changes of, 532
effect of eye-cover on, 532

double (?) cones in, 586

vision through surface by, 435
salmonoids: Salmonidse et al; 384*

adipose lids in, 382-384, 383

anadromous habit in, 372

cornea in, 579

optic nerve and disc in, 179

orbit in, 384

relationships of, 384, 586-587

sclera in, 578
SSlzle, 512-513, 518
Samoiloff, 506
Sand, 539
Sanders, 524
Sangiovanni, 525
saponin, 75

Sarcophilus (mammal: a dasyurid marsupial;
Tasmanian devil), retinal vessels
and possible tapetum lucidum of,
672
saturation (of colors), 84-87*, 92, 95-96*

in dichromasy, 98

in peripheral vision, 355, 503
saurel: Trachurus, q.v.
Sauropsida: reptiles -i- birds; 139*
sawfish: Pristis, q.v.

Scalopus (mammal: a mole), eyes of, 677
Scaphiopus (amphibian: spade-foot toad)

habits of, 418

pupil of, 161, 223

sensitivity of retina in, 161
Scaphirhynchus (chondrostean: shovel-nosed
sturgeon), 136, 569; pupil of, 160,
220, 222
scarlet snake: Cemophora, q.v.
SchieflFerdecker, 191, 591

Schiemenz, 487
von Schiller, 363-364
Schimkewitsch, 131
Schlemm, canal of

absence of, 265, 560, 568, 574, 589
taxonomically:
teleosts, 581

amphibians, 267, 407, 595-596, 610
sauropsidans in general, 668
chelonians, 609-610, 613
crocodilians, 613
Sphenodon, 618-619
lizards, 632
snakes, 628-630, 633
birds, 646
monotremes, 668
marsupials, 674
placentals, 680
man, 7, ID, 12
Schlieper, 492, 495
Schmidt, 515

Schneider-von Orelli, 692 (entry for p. 434)
Schnurmann, 481
Schultze, 64, 191, 215, 611
Schwalbe, 'green' rod of, 55, 58*, 599-600,
Schwarz, 685 [603, 605

Scincidas (reptiles: a lizard family)
conus papillaris in, 625
fovea in, 188
lid windows in, 457
SciuridcB (mammals: squirrels, q.v.)
Sciurus (mammal: squirrel)
color vision in, 513-515
optic disc in, 180
sclera

cartilage of

distribution of, 569
evolutionary origin of, 557
loss of, and eyeball shape, 417, 671
taxonomically:
elasmobranchs, 563-566, 564-565
sturgeons, 569-570
cladistians, 589
holosteans, 574
teleosts, 577^-578
dipnoans, 590
anurans, 594-595
urodeles, 601-602
sauropsidans in general, 270
chelonians, 609
crocodilians, 613
Sphenodon, 617-618
lizards, 623, 632
birds, 643, 645
monotremes, 284, 666 667
marsupial, 671
evolutionary origin of, 119, 557
irregular bones in, 274, 595

INDEX AND GLOSSARY

773

ossicular ring in

oligomeric (i.e., with few units), of
fishes, 271, 274, 380-381, 578-
579, 586
polymeric (i.e., with many units), of
sauropsidans, 270-271, 274-276,
275, 280, 381, 437, 441, 609,
617-618, 623, 632, 642-645,
666, 681
thickenings of, 441, 445-446, 563-566,
627, 678
eye size and, 415-417, 569-570
visibility in lid opening of
in mammals in general, 311
in sirenians, 408
taxonomically:
lampreys, 556-557
elasmobranchs, 564-566, 563
sturgeons, 569-570
holosteans, 574
teleosts, 578-579
dipnoans, 590

amphibians, 594-595, 601-602, 606
chelonians, 609
crocodilians, 613
Sphenodon, 617
lizards, 623
snakes, 627-629
birds, 642-644
monotremes, 666
marsupials, 671-672
placentals, 677-678
whales, 415-417
man, 7-9, 8
Scomber (teleost: mackerel)

falciform process, campanula, in, 583
head and adipose lids of, 382
scombroids: mackerels etc.
adipose lids of, 382-383
guanin in retinae of, 585
visual cells in, 586
Scopelus: Myctophum (q.y.), in part; 405
Scophthalmus (teleost: a flatfish; turbot),
eye and pupillary operculum of,
ScoTpana (teleost: scorpionfish ) [158

stripes crossing eye in, 546
visual cells in, 586-587
scotocyte, 53*

scotoma: an area of invisibility within the
central, 97 [visual field

perception of motion in, 343
physiological, 178-179*, 179-180
filling-in of, 332

movement-perception and, 366-367
multiple, 367
scup: Stenotomus, q.v.
Scylliorhinus (elasmobranch: spotted dog-
habits of, 222, 429 [fish)

lids and photophobia in, 429
loss of optic pedicel by, 564
pupil of, 222, 224-225, 228, 256, 273
sea-horse: Hippocampus, q.v.
sea-lions: eared seals; Otariidae; eyes of,

445-446
sea-snakes: Hydrophiini, q.v.
seals (-(- walrusses = Pinnipedia, q.v.)
Sebastodes (teleost: rockfish), visual cells
Secerov, 526 [of, 586

Selache (elasmobranch: basking shark)
habits of, 222, 243
pupil of, 220, 222

tapetum lucidum (lacking) in, 240, 243,
thick sclera of, 569 [568

sensitivity (see also nocturnality, adaptations
for), 65*
adaptations in deep-sea fishes for, 395-407
apparently unnecessary, of seals, 446-448
factors in, 65

retinal, 53, 68-71
nocturnality and, 206
ocular proportions and, 210-214
summation and, 65, 69
time in darkness and, 71, 73
Selachii (elasmobranchs: sharks -i- batoids,

qq.v.), 135-136*
Semotilus (teleost: a cyprinid; dace), color

vision of, 473, 486
Sepedon (reptile: a spitting cobra), visual

cells of, 178, 637-638
Seps (reptile: a scincid lizard), ciliary

muscle of, 619, 624
SerranidcB (teleosts: true [sea-] bass family),

side-resting habit in, 385
S err anus (teleost: sea-bass)
aphakic space in, 261
binocular field in, 292
eye in, 185, 261
fovea in, 185, 304
optic nerve in, 261
sessile: said of organisms which live attached
Seton, 246 [to a substrate

Seymouria, 607*
Sgonina, 512, 517
shad: Alosa, q.v.

sharks: selachian elasmobranchs, except rays
accommodation and refraction in, 251, 259-
260, le-y-iei, 272-273, 381, 429
area centralis in, 184-185, 187, 243, 245
chorioid in, 243-244, 566
ciliary body in, 262, 372, 567
cornea in, 566

dermal color changes in, 537
distribution of, 563
eye in, 259

shape of, 380, 565
size of, 386, 563

774

INDEX AND GLOSSARY

sharks — cont'd

habits of, 200, 219, 222, 372, 429, 563,

iris in, 567 [568

lens in, 567

lid-complex in, 382, 386, 428-429, 563

mydriatic pupil rigor in, 159

oculorotatory muscles of, 303, 564-565

open embryonic fissure in, 265

optic nerve in, 569

optic pedicel in, 564-565

orbit of, 564-565

pupils of, 150, 159, 219-220, 222, 224-

retina in, 568 [225, 256

scleral thickness in, 415-416, 564-566, 569

tapetum lucidum in, 240, 243-244

taxonomic position of, 135-136

visual cells of, 150, 184, 561, 568, 688,

692 (entries for pp. 561, 568)
visual fields of, 291, 385, 405
zonule in, 260, 268, 372, 429, 567

BY COMMON NAMES:

basking: Selache, q.v.

cat—: Gingylostoma, Scylliorhinus, qq.v.

deep-sea: Etmopterus, Lcemargus, qq.v.

dogfish-: Mustelus, Scylliorhinus,
Squalus, qq.v.

great blue: Prionace, q.v.

hammerhead : Sphyrna, q.v,

luminous: Etmopterus, q.v.

man-eating: Carcharodon, q.v.

nurse-: Gingylostoma, q.v.

porbeagle: Lamna, q.v.

requin: GaleorhinidcB, q.v.
Sharp, 125
shearwaters

area and fovea of, 187

feeding method of, 439
sheep

accommodation (lacking) in, 285

cheek-stripe in, 546

corpora nigra of, 227

interpupillary distance of, 327

woolly cornea in, 453
shell, visibility of, 351
shiner: Notropis, q.v.
shore birds, head movements of, 342
shrews (mammals: lipotyphlous insectivores)

eyes of, 680
size of, 677

Harderian gland in, 426

taxonomic position of, 676

visual cells of, 685
shrike, use of in falconry, 169
Sichel: Pelecus, q.v.

SiluridfB (teleosts: a catfish family), refrac-
tive index of lens in, 265
siluroids (teleosts: catfishes)

cavemicolous, 387-388, 390

chorioid gland (lacking) in, 581
imitators of, 460
pupillary operculum in, 158, 160
retina in, 147, 176, 585

photomechanical changes of, 147
spectacles in, 450
upside-down swimming in, 523
visual cells in, 147, 586
Simenchelys (teleost: parasitic eel), eye and

habits of, 391
Simice: Anthropoidea, q.v.; 228*, 515*
Sims: ciliary web, q.v.
Sinclair, 664
singleness, 315-338 (see also binocular vision,

fusion, stereopsis)
Siphonostoma (teleost), fovea in, 304
Siren (amphibian: a sirenid urodele), eye

and habits of, 407
Sirenia (order of mammals: sea-cows;
Dugong + Trichechus, qq.v.)
accommodation and refraaion in, 272-273
as basis of 'mermaid' legend, 407
ciliary body, shape of, in, 286
compared with:
crocodilians, 422
hippopotamus, 443
monotremes, 669
seals and whales, 408, 412
eyes and vision of, 407-410, 409
habits of, 368-369, 407-409
lashes of, 426
necklessness of, 377
taxonomic p)osition of, 676
SirenidcE (amphibians: a urodele family),

eyes and habits of, 600
size, perception of, 247-248, 344
size of eye

and body, 172

and spectacle, 453

and speed, 174

and thickness of sclera, 415

taxonomically:

lampreys, 556

hags, 562

elasmobranchs, 386, 563

deep-sea, 397-399
gars, 574
teleosts, 432

deep-sea, 212, 395, 397-399
dipnoans, 590

amphibians, 407, 600, 605-606
crocodilians, 613
Sphenodon, 617
lizards, 617, 620, 622-623, 625
blind snakes, 627

birds, 172-173, 212, 307, 641-643, 650
monotremes, 666
marsupials, 673-674

INDEX AND GLOSSARY

775

placentals, 171-173, 211-212, 677-678
sirenians, 408
whales, 171, 210, 415-417
seals, 445
size-weight illusion, 530*
skates (+ rays = Batoidea,^.r.)
skin

color changes in (see color changes)
photosensitivity of, 128-129
skinks: Scincidae, q.v.
skunk, exophthalmos of, 426
sleepers: gobies, q.v.

slit-lamp microscope: a low-powered binoc-
ular microscope employed with a
slanted, ribbon-like beam of light
for studying the structures of the
living anterior segment
Slome, 538
sloths

eyeshine in, 241
movements of, 270
pupil in, 221

taxonomic position of, 139, 676
two-toed: Cholapus, q.v.
Smith, E. M., 506

Smith, G. E., 312, 692 (entry for p. 312)
snake venom, as solvent for rhodopsin, 75
snake-birds, feeding method of, 439
snake-eyed lizard: Ophiops, q.v.
snake-lizards: Pygopodidae, q.v.
snakes (suborder Ophidia of reptilian order
Squamata)
accommodation and refraction in, 251,
272-273, 282-283, 299, 438,
456, 630-631, 633
aquatic and amphibious, eyes of, 438
area temporalis and fovea in, 185-188,

186, 283, 307, 635
binocular vision in, 299, 306-307
canal of Schlemm in, 628-630, 633
chorioid in, 629, 654
ciliary body in, 629, 633, 673, 680
color vision in, 497, 519-520
coloration of eye in, 545-547, 549
conus papillaris in, 631, 633-635
cornea in, 627-628
dermal color changes in, 542-543
distribution of, 622
eyes of, 456, 627-640, 633
movements of, 306-307
reconstrurtion of, 608, 632-636, 687
eyeshine in, 230, 240
habits of, 150, 162, 165-166, 169, 174,
199, 201, 203-204, 225, 270, 293,
295, 344-345, 438, 450, 458-
459, 633-640
Harderian gland in, 424, 455-456, 635
iris in, 630, 633, 635

lacrimal system of, 424, 455
lens in, 438, 456, 628, 630-635, 633
yellow coloration of, 168, 191, 199,
201, 203-204
movement-perception by, 344-345
ocular proportions in, 174, 627, 633, 666,
optic axes in, 294 [671

optic nerve in, 632, 635
origin and ocular history of, 203, 458-

459, 632-636
pupils of, 150, 157, 161-162, 165-166,
168, 176, 220-221, 225, 257,
272-273,299,438
relationships of, 135, 138, 622, 632, 636
retina in, 167-168, 178, 634-640, 636,638
photomechanical changes (lacking) in,
150, 166
sclera in, 627-629, 634
spectacles of, 424, 450-451, 454-455, 456-

459, 628, 633-634
visual acuity in, 169, 174, 178, 344, 497
visual cells of, 56, 59, 61-63, 157, 161-
162, 165-169, 166-167, 176, 178,
201, 216, 497, 634-640, 636-639,
688-689
rhodopsin (and its absence) in, 78,

166, 168, 636, 638
zapfensubstanz in, 101-102
visual fields of, 293-295, 299
vitreal vessels in, 631, 633, 654
zonule in, 629-631
snapping turtle: Chelydra, q.v.
snipes

binocular field in, 295-296
pupil in, 227
Snow-White and the Seven Dwarfs, 360
Soemmering, 191
soft-shell turtle: Amyda, q.v.
soles: Soleidse, q.v.
Soleidas (teleosts: a flatfish family; soles),

vestigial eye in, 210
solidity, perception of (see stereopsis), 315*
song-birds (see Passeriformes)
Sonora (reptile: a colubrid snake), scleral

pigment in, 628
sooty mangabey: Cercocebus, q.v.
souslik: Citellus, q.v.

space, perception of, 247-248, 288-388, 341-
367 (see also binocular vision, dis-
tance, eye-movements, local signs,
movement, size, stereopsis, visual
fields)
value of vision in, 288, 343-345
spade-foot toad: Scaphiopus, q.v.
Spalax (mammal: mole-rat), eyes of, 210,
spectacle, 449* [677

distribution, functions, and types of,
450 (Table XI)

776

INDEX AND GLOSSARY

spectacle — cont'd

primary, 258, 380, 419, 436, 449*-453,
451, 556, 593, 604, 606
conversion of, into conjunctiva, 259,
451-452,579
secondary, 432, 449*, 453-454, 459-460,
tertiary, 449*, 451 [579,590

fishes, 383, 454, 459-461
reptiles, 418, 423, 427-428, 454, 455-
457, 458-459, 625, 627, 633-634
spectrum
absorption-, of water

rhodopsin and, 373-375, 462
equal -energy, 91
grand, 4 (Table I), 462
neutral point in, 98
photopic, 92-93, 195
physical, 82

psychological, 82, 94, 462
scotopic, 91-92
transmission-, of ocular media, 194, 196,

199, 462, 521
visible, 462

limits of, in man and animals, 462,
471, 491, 494-498
speed, vision and (see also movement),
345-347
ocular size and, 174, 346
spermophile (see squirrels, ground-)
Sphcerodactylus (reptile: a spectacled gecko)
diurnality in, 203, 627
eye- and body-size in, 203
pupil in, 203, 220, 627
visual cells of, 627
Sphceroides (teleost: puffer), eye-movements,
pupil, and possible fovea of, 304-
Sphenifcus (bird: a pjenguin) [305

binocular field (lacking) in, 291, 295
monocular fixation by, 295
Sphenodon (reptile: sole living rhynchoceph-
alian), 692 (entry for p. 270)
accommodation in, 272-273, 619-621
adnexa of, 420-421, 458, 617
binocular vision in, 306
bridge-membrane of, 618-619, 624
chorioid of, 617

ciliary body of, 618-619, 623-624
color vision (?) in, 497, 519-520
conus papillaris in, 620-621, 653, 657
cornea of, 617
eye of, 616-621, 618

compared with lizard, 616-617, 622-623
departure of, from standard reptilian

pattern, 622
size and shape of, 617, 620
fovea in, 187-189, 202, 620-621

chorioidal pigmentation opposite, 617
habits of, 150, 200, 657

iris of, 617-620, 647
lens of, 618-621
optic nerve of, 620-621
parietal eye of, 340
pupil of, 220, 224, 621

mobility of, 150
retina of, 189, 620-621, 623
scleral cartilage of, 617-618
scleral ossicles of, 270, 274, 617-618, 620
taxonomic pjosition of, 138, 616
visual acuity of, 206
visual cells of, 150, 621

compared with other sauropsidans, 616,

621, 661
cone-origin of rods, 167, 190, 497, 520
oil-droplets of, 200, 202
rhodopsin (lacking) in, 78
vestigial character of cone population,
150, 216, 621, 623, 661
Sphyrna (= 2yg<r«d; elasmobranch: hammer-
head shark)
'nictitating membrane' of, 563
optic pedicel of, 564
pupil of, 222
spider monkey: Ateleus, q.v.
Spinachia (teleost), color vision in, 473
Spinax: Etmopterus, q.v.
spoonbills: Polyodon, Psephurus, qq.v.
spotted dogfish: Scylliorhinus, q.v.
spotted jewfish: Promicrops, q.v.
spotted night snake: Hypsiglena, q.v.
sprat, falciform process in, 582
Squalus (elasmobranch: dogfish)
Descemet's layers in, 566
mydriatic pupil rigor in, 159
osmotic pressure of aqueous in, 372
Squamata (order of reptiles: lizards + snakes,

qq.v.), 622*; eyes of, 622-640
Squatina (elasmobranch: monkfish, angel-
habitus of [fish)
and eye aim, 385
and pupil, 222
lid-complex in, 386
visual cells of, 568
squint: in the lay sense, looking through
partly-closed lids; in the technical
sense, a fixed convergence or diver-
gence of the optic axes — cross-
eyedness (= strabismus, q.v.)
squirrel monkey: Saimiri, q.v.
squirrels: rodent family Sciuridae (see also
Marmota, Sciurus)
accommodation and refraction in, 287,
area centralis in, 187 [681-682
color vision in, 513-515
coloration of iris in, 545
eye-movements of, 312
eyeshine in, 230

INDEX AND GLOSSARY

777

flying- (see also Glaucomys, Pteromys)
imitation of, by marsupial types, 664

(see also Petaurus)
imitation of, by non-sciurid rodents,

664 (Anomalurid£e)
optic disc in, 1 80
retinal vessels in, 201, 654, 658
visual cells in, 55-56, 166, 176, 685
visual cortex of, 523
ground- (see also Citellus, Cynomys)
color vision in, 514-515
immunity to dazzlement of, 205
pupil and habits of, 162
pure-cone retinee of, 176, 513-514
universal macularity of, 190, 312
habits of, 162, 201, 204-205, 227, 312,

504, 508, 658
lens in, 174 [504, 508, 658

yellow coloration of, 191, 199, 201, 203
optic axes in, 297
optic nerve in, 179-180, 367
pupil in, 227

retina in, 176-177, 685-686
layers of, 684-685
vessels of, 684
size of eye in, 170
activity and, 174
visual acuity of, 312
visual cells of, 685-686
visual cortex of, 523
visual fields of, 296, 312
zonule in, 682
stalked eyes, 403-405, 404
Stampfer, 357

stargazers: Uranoscopidae (^.v.), et al
Stark, 525
Steatornis (oil-bird)
eyeshine in, 240
habits of, 201, 500, 545
iris coloration of, 545
oil-droplets of, 201
possible lack of cones in, 500
pupil of, 226
Stegocephali (extinct amphibians ancestral
to reptiles; -i- Lissamphibia = Am-
phibia); 137*, 137
characteristics of, 137, 208
color vision in, 518-519
median eyes of, 137, 339
probable habits of, 600
relationships of, 137-138, 593, 601
scleral ossicles of, 274
visual cells of, 600, 603
stenopaic aperture (or pupil), 224*, 224,
386
accommodation and, 255-257, 438
from crossed pupil and lids, 428
from slit pupil -i- astigmatism, 447-448

Stenotomus (teleost: scup), eye-movements,
pupil, and possible fovea of, 304-
305
step-wise phenomenon, 470*, 473, 475
Stereocydops: Hypopachus (in part), q.v.
stereopsis, 315*

basis of, 320-326, 331-338

in man, 315-319

monocular, 323, 341-342

suppression of vision for, 349
stereoscope, 315-316, 324, 331-332, 333-334
stereoscopic motion piaures, 361
stereoscopic visual acuity, 331*
Sternoptychidee (teleosts: a lantern-fish

habits of, 402 [family)

retina in, 399
sticklebacks: Eucalia, Gasterosteus (qq.v.),

et al; falciform process in, 582
Stizostedion (teleost: a percid; pikeperch,

habits of, 374 [walleye)

horizontal cells of, 585

retinal tapetum lucidum of, 236

visual cells of, 587
stone-curlew: Burhinus, q.v.
strabismus, 329*-330 (see also squint)
Stratton, 505

streamlining of eye, 377, 379-384, 461
strigine: pertaining to owls
Strigops (bird: owl-parrot, kakapo)

area temporalis of, 187

binocularity of, 295

habits of, 201, 295

oil-droplets of, 201

pecten of, 657
Strix (bird: an owl), visibility of infra-red
stroboscope, 357*, 357-358 [to, 502

Struthio (bird: ostrich)

eyeshine of, 230, 240

lamina vitrea of, 230

largest terrestrial eye, in, 642

mobile upper lid of, 424

pecten of, 649, 656-657

ringwulst in, 648
Studnicka, eye-origin theory of, 126-128
von Studmtz, 100-102, 151, 495
sturgeons: Acipenser, Huso {qq.v.), et al

shovel-nosed: Scaphirhynchus, q.v.
Stygicola (teleost: a cave brotulid), eye and

ecological history of, 388
'Stylopkhalmus, 403-405, 404
substrate, protection of eye from (see spec-
tacle)
Suina (mammals: pig-peccary-hippopotamus
division of artiodaayl ungulates;
see also Hippopotamus)

accommodation (lacking) in, 285

anterior segment in, 683

iris muscles in, 678

778

INDEX AND GLOSSARY

Suina — cont'd

mucous tears in, 426

optic axes in, 297

tapetum lucidum (lacking) in, 241

taxonomic position of, 676
Sula (bird: booby)

feeding method in, 439

sexual difference in iris of, 226, 550
summation (retinal), 47*-48, 66-70

acuity and, 67

in circles of innervation, 350

local reduction of (in area centralis), 182

physiological increase of, 80

in relation to habits, 175-178, 177, 216-

sensitivity and, 69 [217

taxonomically:

elasmobranchs, 568

sturgeons, 572

teleosts, 585
deep-sea, 400

urodeles, 603

csecilians, 606

chelonians, 611

snakes, 639

birds, 659, 661

monotremes, 670-671

placentals, 685
man, 67-68
Sumner, 482, 524, 526-527, 530-532, 534-
sunfish [535

freshwater: see Centrarchidse, Lepomis

ocean: Mola, q.v.
superior colluculi, 329, 335, 522*
suprachorioidea (see chorioid)
Suricata (mammal: a viverrid carnivore;
suricate)

diumality of, 686

pupil of, 221, 227

binocular field and, 299

tapetum lucidum (lacking) in, 241

vegetarianism of, 227
susa: Platanista, q.v.

swallowing, use of eye in, 305, 594, 601
swallows

area and foveje of, 187, 189, 307

oil-droplet colors in, 197

visual field of, 295, 307-308

visual trident of, 307-308
swan: Cygnus, q.v.
swifts: Apus {q.v.) et al

accommodation in, 655

oil-droplet colors in, 197

as owl ancestors, 309

peaen in, 655
swordfish, Xiphias, q.v.
Sylvius, aqueduct of: the canal which con-
nects the third and fourth ven-
tricles of the brain; 302

syncitial: said of tissues in which cell-mem-
branes are lacking, so that there
is a continuum of cytoplasm in
which many nuclei are distributed
Synentognathi (teleosts: flyingfishes -i- half-
beaks -I- needlefishes)
relationships of, 576
ventrad tilt of eyes in, 293, 296
Syngnathus (teleost: pipefish)
color vision of, 473
falciform process of, 582
fovea of, 304
sclera of, 578
Synodontis (teleost: upside-down catfish;

batensoda), reversed coloration of,
Szepsenwol, 530, 536 [523

Tachyglossus (mammal: an echidna)

habits of, 201

ocular structure in, 664-671, 667, 670

pupil of, 221

taxonomic position of, 663

visual cells of, 201, 670-671, 688
taguan: Pteromys, q.v. (see also 692, entry

for p. 676)
Talpa (mammal: a mole), eyes of, 677
tapetum lucidum, 229*

area centralis and, 243, 245

in birds (?), 646

chorioidal, 231-236, 238-246, 678
cellulosum, 232, 233-235*
fibrosum, 231*, 232-233, 672
guanin, 238-239, 242-244, 570-571, 589

distribution of, 240-241 (Table VII),
398, 568, 672

efficiency of, 243-245

in primates, diversity of, 517

phylogeny of, 243-245, 571

retinal, 231, 233, 235, 237-239, 245, 585,
615-616, 672, 684, 692 (entry for
p. 236)

retinal nutrition and, 654, 672

special funaion of, in seals, 446-448

visual acuity and, 245-246
tapirs, optic axes of, 297
Tar bo phis (reptile: a colubrid snake)

habits of, 166

visual cells of, 166, 638

visual fields of, 294

vitreal vessels of, 63 1
Tarenlola (reptile: a spectacled gecko)

lens of, 620

pupil and iris musculature of, 223
Tarpon (teleost)

adipose lids (lacking) in, 383

leptocephalus stage of, 406
tarsier: Tarsius, q.v.

INDEX AND GLOSSARY

779

Tarsius (mammal: a lemuroid)
color blindness of, 520
relationships of, 517
rotatability of head of, 213, 309
stenopaic pupil of, 162, 221, 228, 257, 273
tapetum lucidum (lacking) in, 241
tubular eyes of, 309, 677-678
immobility of, 213, 309
Tauredophidium (deep-sea teleost), vestigial

eye of, 397
taxonomy: the Isranch of biology which deals
with the classification of organisms
in accordance with their evolution-
ary history and relationships
tears, properties of, 41, 678
tegmentum: a portion of the brain; 302*,
TeiideB (reptiles: a lizard family) [329

ciliary muscle in, 624
spectacles in, 450
teleost fishes: Teleostei; 135, 137*

eyes and vision of: sub-index, p. 573;

575-588;
and:

argentea of, 570
chorioid of, 651
ciliary folds in, 567
falciform process of, 653
retina in, 659

tapetum lucidum in, 692 (entry for p.
vitreal vessels of, 652-653 [236)

telescopic eyes: tubular eyes, q.v.
Telmatobius (amphibian: an anuran), com-
pletely aquatic habits of, 368
TelosauridcE (reptiles: extinct crocodilians),

upward aim of eyes in, 274
ten-pounder: Elops, q.v.
Teratolepis (reptile: a spectacled gecko),

pupil and visual cells of, 627
terns

areae and foveae of, 187
feeding method of, 439
terrapins: amphibious chelonians, q.v.
terrestrial activity

'adaptations' for, in elasmobranchs, 428-

429
adnexal requirements for, 418, 592-593
dioptric requirements for, 417
eyes and vision in, 417-429
Testudo (reptile: a tortoise)
accommodation in, 437
binocular field of, 293-294
eye of, 609
lens of, 437, 620
scleral ossicles of, 274
sexual difference in eye color of, 550
transversalis muscle (lacking) in, 437
Tetragonopterus (teleost: tetra), bony sclera
of, 381, 578

Tetrodon (teleost: a globefish), fovea of,

304
thalamus: portion of the brain alongside the

third ventricle
Thalassochelys (reptile: a sea-turde), an-
terior segment in, 437
Thamnophis (reptile: garter snake)
abrasion of spectacle in, 456-457
visual fields of, 294
Thelotornis (reptile: a colubrid; African
bird-snake)
accommodation in, 283
binocular vision in, 283, 307
fovea in, 186-187, 299, 307
pupil of, 186, 221, 299
relationships of, 299
Therapsida (extinrt reptiles ancestral to mam-
mals), 135; cones and color vision
in, 519-520
thermocline: an intermediate layer of water
in lakes, within which the temper-
ature changes regularly with depth
Thieulin, 298

third dimension, perception of (see bathop-
sis, stereopsis), 313*
motion pictures with, 361
Thompson, A., 296, 550
Thompson, D., 528

Thoracochorax (teleost: a characin; hatchet-
fish), 'flight' of, 431
threshold of stimulation, 65, 69*

by moving objects, 347
throat-fan, 525

Thunnida (teleosts: tuna family)
guanin in retina of, 585
visual cells in, 586
Thunnus (teleost: tuna)

coloration and habits of, 528
scleral ossicles of, 271, 380-381
Thylacinus (mammal: marsupial 'wolf),

tapetum lucidum of, 241, 672
Tierra del f^uego, visual acuity in natives of,
tiger (a felid) [190

outer nuclear layer of, 217
protective coloration of, 523
taxonomic position of, 139
Tiliqua (reptile: a scincid lizard)
lid window of, 450
visual fields of, 294
tinamou

flying capacity of, 648
pecten in, 649
taxonomic position of, 650
Tinea (teleost: a cyprinid; tench), cone-
concentration in, 176
toadfish: Opsanus, q.v.
toads: Anura (in part), q.v.
toddy cat: Paradoxurus, q.v.

780

INDEX AND GLOSSARY

Torpedo (elasmobranch: a batoid; electric
pigmented cornea of, 219, 433 [ray)

pupil and operculum of, 220, 222, 386
retina of, 568
torrent ducks: Merganetta spp.; 439
tortoises: terrestrial chelonians, q.v.
Toxotes (teleost: archer-fish)

binocular field of, 292, 304

fovea (lacking) in, 304

habits and eye of, 435
trabeculae: strut-like columns of supportive

tissue
Trachinus (teleost: weever), fovea in, 304
Trachurus (teleost: a scombroid; horse-mack-
erel), binocular field of, 292
Trachycephalus (amphibian: an anuran),

pupil of, 223
Trachysaurus (reptile: a scincid lizard)

lid window of, 450

visual fields of, 294
Tragulus (mammal: mouse-deer, chevrotain )

corpora nigra (lacking) in, 679

retinal vessels of, 684

taxonomic position of, 679, 684
Trautman, 551

tree-frogs, tree-toads: Hylidae and some
smaller anuran families; accom-
modation and habits of, 436
tree-shrew: Tupaia, q.v.
tree-snake. East Indian long-nosed: Dryophis,
Trendelenburg, 91, 515 [^.v.

TretjakofF, 597; eye-origin theory of, 130-133
Trichechus (mammal: manatee)

as basis of 'mermaid' legend, 407

eye and vision of, 408-410, 409
' pupil of, 447
Trichosurus (mammal: cuscus)

anterior segment of, 673

cornea of, 671

habits of, 227

optic chiasma of, 319

pupil of, 221, 227
Trigla (teleost: gurnard)

binocular field of, 292

dermal color changes of, 481
Trimeresurus (reptile: a crotalid snake),

optic axes of, 294
Trimorphodon (reptile: a colubrid snake)

fibrous tunic of, 628

retina and pupil of, 168

visual cells of, 63, 168, 638
Trionychoidea (reptiles: soft-shelled turtles) ,
tritanopia, 99* [fovea in, 612

Triton: Triturus, q.v.
Triturus (amphibian: newt)

cartilage and bone in sclera of, 274, 601

dermal color changes in, 536

ocular camouflage in, 546-547

retinal summation in, 603
visual cells of, 603
Troglichthys (teleost: an amblyopsid),

degenerate eye of, 387
Tropidophis (reptile: a bold snake)
canal of Schlemm in, 629-630
fibrous tunic of, 628
retina of, 167, 636
trout: SalmonidjB (in part), q.v.
trunkfishes: teleost family Ostraciidae
falciform process (lacking) in, 582
peculiar comecE of, 580
vitreal vessels of, 582-583
Trygon (elasmobranch: a sting ray), pupil-
lary operculum of, 386
Trypauchen (teleost: a goby), degenerate

eye of, 210, 387
tubular eyes, 212-213, 400-403, 642-643,
677-678
accessory retinae of, 257, 400-401
accommodation in, 262
Matthiessen's ratio in, 264
ontogeny and phylogeny of, 400-403, 401
upward aim of, 402-403
Tubulidentata (order of mammals: 'eden-
tates' [in part]; see Orycteropus) ,
tuna: Thunnus, q.v. [676*

Tupaia (mammal: tree-shrew)
diurnality of, 199, 201, 517, 676
possible color vision of, 517
retina and visual cells of, 201, 685-686,
taxonomic position of, 139, 517 [688

yellow lens of, 191, 199, 201
Tupinambis (reptile: a teiid lizard), ciliary

muscle of, 624
turbot: Scophthalmus, q.v.
Tardus (bird: thrush genus containing

American 'robin'), retina in, 659

turkey, eye of, 420, 650

turtles: reptilian order Chelonia (^.v.); or

(in strictest sense) marine chel-

Twain, 658 [onians

two-point limen: the angle subtended at the

eye by two points which can just

be seen to be separate; in man, 350

Tylopoda (mammals- camels, llamas, etc.),

676*; tapetum lucidum in, 241
Typhlachirus (teleost: a flatfish; blind sole),

vestigial eye of, 210
Typhlias (teleost: a cave brotulid), ecolog-
ical history of, 388
Typhlogobius (teleost: Californian blind
adhesive disc of, 432 [goby)

commensalism (with shrimp) of, 388
experimental pigmentation of, 533-534
Typhlomolge (amphibian: a cave salaman-
degenerate eye of, 407 [der)

occasional scleral cartilage of, 602

INDEX AND GLOSSARY

781

Typhlonarke (elasmobranch: a deep-sea

ray), vestigial eye of, 397
Typhlonectes (amphibian: a cacilian),

unique aquatic habit of, 605
Typhlonus (deep-sea teleost), vestigial eye

of, 397
Typhlopids (reptiles: a fossorial snake
eyes of, 627 [family)

spectacles of, 450
Typhlops (reptile: a typhlopid snake)
eye and lacrimal system of, 424
possible primitiveness of, 635-636, 691
(Plate I)
Typhlotriton (amphibian: a cave salaman-
degenerate eyes of, 407 [der)

recrudescence of, 390
lids of, 450, 458
scleral cartilage in, 602
unique metamorphosis of, 602

von Uexkiill, 351

ultra-violet (see light), 4

Umbra (teleost: mud-minnow), color vision

of, 467, 483-484, 486
umbraculum (see pupil)
ungulates (hoofed mammals), 676*; see
also Artiodactyla, Perissodactyla
accommodation and refraction in 285,

287, 680
area centralis in, 185, 187, 245, 292
ciliary body in, 679, 681, 683

muscle of, 285, 680
color vision in, 505
cornea in, 671

corpora nigra of, 219, 221, 227, 679
evolution of, 283, 504-505, 676
eye-movements in, 311
habits and visual acuity in, 170, 353
intra-ocular color-filters (lacking) in, 203-
iris in, 678-679 [204

lens in, 684

nasad asymmetry of, 173, 300, 678-679
nictitating membrane in, 427
optic axes of, 297
pectinate ligament in, 680
pupil m, 218, 221, 227, 245, 256, 299
retinal vessels in, 654, 684
shape of eye in, 677-678
size of eye in

habits and, 145, 176, 245, 504, 677
retinal image and, 176, 245
speed and, 174

tapetum lucidum and, 145, 245
tapetum lucidum in, 145, 231-234, 239,

241, 245-246
visual cells in, 685, 688
visual fields of, 297-299

uniocular fields, 291*

cortical projection of, 334-335
isolation of, 321-322
shape of, 298
universal macularity, 312*
UranoscopidjE (teleosts: stargazer family)
elevation of eyes in, 438
habitus and eye aim in, 385
pupil in, 150, 158, 220
Uranoscopus (teleost: stargazer)
dorsal binocular field of, 293
pupil in

mobility of, 160
operculum of, 158, 386
Urodela (tailed amphibians: salamanders,
newts, etc.)
accommodation and refraaion in, 266-267,
272-273, 407, 597, 692 (entries
for pp. 266, 273 )
adnexa in, 419, 601
cavernicolous {Haideotrtton, Proteus,

Typhlomolge, Typhlotriton) , 210,
300, 390, 407, 453, 458, 600
classification of, 600
color vision (?) in, 490
cornea in, 601-602

dermal color changes in, 526-527, 537-538
ependymal cells of, 56, 573
habits of, 150, 200, 266, 368, 407, 418,
iris and body coloration in, 545 [653

lens in, 601-602
multiple optic papilla in, 367
permanently aquatic, 407, 419, 600
protractor lentis muscle in, 272, 602
pupils of, 150, 220, 223, 692 (entries

for pp. 266, 273)
relationship to anurans of, 593, 601
retina in, 603, 653

photomechanical changes of, 150, 152
sclera of, 417, 601-602

bone in, 274
size and shape of eye in, 417, 600-601
spectacle in, 449, 453
uvea in, 602

visual cells of, 200, 572, 599-600, 603
visual field of, 293
zonule in, 602
Uromacer (reptile: a colubrid snake),

binocular field of, 294
Uromastix (reptile: an agamid lizard;
lens in, 620 [mastigure)

ocular proportions in, 617
Uropeltids (reptiles: a primitive and fos-
sorial snake family), 201
Uroplatus (reptile: monotype of a lizard fam-
habits of, 200 ily very close to

pupil of, 220 the Gekkonidae)

spectacle of, 450

782

INDEX AND GLOSSARY

Uta (reptile: an iguanid lizard), habits and
pale dermal phase of, 541

uvea, uveal traa: chorioid + ciliary body +
iris, qq.v.

vacuole: a small, fluid- (rarely, gas-) filled
cavity within a cell or (in loose
sense) in a tissue
Valentin, 183
Vanderplank, 502
Vanellus (bird: lapwing), embryonic head

of, showing corneal sensills, 271
VaranidcB (reptiles: a lizard family whose
only living genus is Varanus, g.y.)
as ancestors of snakes, 632-634
Varanus (monitor lizards)

area temporalis and fovea of, 187
chorioid of, 617
retina of, 625
size of, 293

visual fields of, 293-294, 306
anterior blind cone of, 298
vascular, vascularized: supplied with blood

vessels
ventrad: toward the ventral side (of an
Verrier, 215, 304, 586, 685 [animal)

vertigo, disturbance of reflex eye-movements

in, 301
Vipera (reptile: a viperid snake; common
conus papillaris of, 631 [adder)

sexual difference in eye color of, 549
visual cells of, 640
visual fields of, 294
Viperidffi (reptiles: a snake family; Old-
World vipers)
habits in, 201
pupil in, 221, 225
visual cells in, 639-640
vipers: Viperidje, q.v.

pit-: CrotalidcE, q.v.
Virchow, 657

vision (see also binocular vision, color vision,
movement, sensitivity, space, visual
acuity, visual fields)
achromatic, 64-65*

acute, diurnality and, 169-175, 464-465
after cataract extraction, 204
anomalous trichromatic (see color blind-
compensations for loss of, 388 [ness)
dependence on rhodopsin of, 75
latent period of, 350
multiplex, 198, 497, 502-503
photopic (see also Purkinje phenomenon),
64*, 81-103, 245
movement-perception in, 352-356
spectrum in, 87, 92-94, 101-102, 462-
refractory period of, 350-351 [464

scotopic (see also Purkinje phenomenon),

64*, 74-80, 245, 464

in deep-sea environment, 395-403

movement-perception in, 352-356

spectrum in, 87, 91-92, 101-102

suppression of, 348-349

through

air (see terrestrial artivity)

air and water (see amphibious aaivity)

fog etc., 197-198, 248

water (see aquatic activity), 462

tube, 214, 445

with tapetum lucidum, 245-246
visual acuity, 53, 65*

accommodation and, 283-284, 588

in achromatic vision, 97

in area and fovea, 181-190, 588

binocular, 308, 331*-333

in birds, 642, 661-662

color vision and, 464-465, 493, 588

color-filters and, 193-198, 204-205

in deep-sea fishes, 398

diurnality and, 169-175, 207, 209

of human races, 190

intensity and, 71-72, 80

in man and animals, 207 (Table V), 246,

in monochromatic light, 89 [662

movement and, 174, 349-356, 365-367, 464

nocturnality and, 206-207, 210-211

optomotor reaction and, 302, 492-493

retinal factors in, 65-68

in sirenians, 409

speed and, 174, 349-367

stereoscopic, 3 3 1 *

summation and, 67

tapetum lucidum and, 245-246

two-point limen of, 350

voluntary eye-movements and, 303-312
visual axis, 7, 292*

alterability of, 299-300, 405, 431, 624
(and see muscle, transversalis)
phylogenetic, 402-403

of amphibious mammals, 443-444

of whales, 413
visual cells (see also Plate I, p. 691)

accommodation and, 30-31, 249, 253-254,
268, 281, 414-415

ancestry and homologies of, 79, 163, 464-
465, 572-573

in area and fovea, 181-184, 195, 692
(entry for p. 195)

compared with half-tone, 332

deficiency of, in achromasy, 97

development of, 107-108

in diurnal animals, 175-178, 177

metabolic requirements of, 648-659, 672,
684

migrations of, 146-148, 149-153, 160-163

INDEX AND GLOSSARY

783

mosaic of, 57, 587-588, 620, 638

in nocturnal animals, 177, 206, 215-217

oil-droplets of, 191*

color ratios of, 197-198, 661

development of, 600

distribution and colors of, 200-201

(Table IV)
effect of, on contrast and color, 196,

496, 501-504
first appearance of, 572
funaions of, 192-198, 497, 502-503,
red field of, 196, 307 [586

spectral properties of, 198
yellow field of, 196
photochemical substances in (iodopsin,

porphyropsin, rhodopsin, zapfen-
substanz, qq.v.), 74-76, 79, 464,
474-475, 518
shape, significance of, 68-69
in tapetalized areas, 245, 615
transmutation of, 61-63, 164-168,568,591,
600, 603, 621, 626-627, 636-640,
687-689
color vision and, 464-465, 520, 688
partial, 616
types and structure of, 52-63, 54-55, 59,
62-63, 586-588, 591, 603, 606,
636-640, 671, 675, 685-689
taxonomically:

lampreys, 58, 518, 559-560, 561-562
elasmobranchs, 561, 568, 692 (entries for
pp. 561, 568)
deep-sea, 399-400, 568
chondrosteans, 200, 242, 570, 572-573,

612, 626
cladistians, 200, 692 (entry for p. 589)
holosteans, 200, 585-587
teleosts, 146-147, 200, 433-434, 586-588,
deep-sea, 396, 399, 586 [587, 591

dipnoans, 200, 591
amphibians, 148, 200, 598-600, 599, 603,

605-606, 612
chelonians, 200, 611-612, 616, 621, 661
alligator, 200, 615-616, 621, 661
Sphenodon, 189, 200, 616, 621, 661
lizards, 167-168, 200, 621, 615-617, 626
geckoes, 62-63, 168, 201, 203, 216,
254, 520, 626-627
snakes, 165-168, 166-167, 201, 634-640,

636-639
birds, 201, 588, 626, 660-661, 692 (entry

for p. 195)
monotremes, 201, 626, 670-671, 686, 688
marsupials, 201, 626, 670, 675, 685, 688
placental mammals in general, 166, 201,
588, 675, 684-689
man, 43, 54-55, 67, 661
'original', 687-689

seals, 446
sirenians, 410
whales, 414-415
visual consciousness, 1-5

locus of, 335-338, 522-523
visual fields (see also frontality, laterality,
optic axis, periscopy)
in aquatic animals, 376-377, 378-379,

443, 592-593
binocular, 290, 298, 320-321, 322, 334
absence of, 291
aphakic space and, 299
devices for enlarging, 299-300, 307
dorsal, 292-293, 385-387, 443, 666
eye-movements and, 300-312
lid actions and, 425
posterior, 293, 296
shape of, 298
ventral, 293, 303, 387
taxonomically:

fishes, 292-293, 303-305, 376, 385-387,
deep-sea fishes, 402-403 [432

amphibians, 291, 293
reptiles, 291, 293-294
birds, 291, 295-296, 307-310, 309, 323,
mammals, 296-298, 666 [442

constancy of, 303, 348
cortical projection of, 334-335
of hammerhead shark, 405
of lampreys, 291
of monotremes, 666
pupil and, 225
of seals, 444-445
spherical lens and, 213-214
tube, 214
uniocular, 291 *
of whales, 291, 413-414
visual pathway, central, 47, 65, 319-338,

335, 521-523
visual purple: rhodopsin, q.v.
visual trident, 307-310*, 309
special employment of, 442
vitamin A (see also carotenoids), 75, 78,

692 (entry for p. 99)
vitreal (= hyaloid) vessels, 575* (consult
also 648-659, 684)
taxonomically:
cladistians, 589, 605, 653
holosteans, 575, 605, 652-653
teleosts, 577, 582-583, 605, 652-653
dipnoans, 590, 605, 653
anurans, 598, 605
snakes, 631, 633, 684
vitreous humor

accommodation and, 268, 584

of amphibians, 611

cleft of, 261, 582

development of, 113- II 4, 117, 582

784

INDEX AND GLOSSARY

vitreous humor — cont'd

of lampreys, 268, 560

of reptiles, 610-611, 624, 630-631

of teleosts, 584, 61 1

tinting of, in jaundice, 100

vestigial status of, 286

water-content of, 371-373

in zonule, 267, 596
Viverridae (mammals: a carnivore family;

civets etc.), pupils in, 227
Vomer (teleost: a scombroid; look-down),

eye aim of, 293
vomeronasal organ, 424*
vorticose veins, 14, 51*, 558
Vulpes (mammal: fox), tapetum lucidum

of, 232
vultures, areee, foveje, and habits of, 187,307

W
Wagner, H., 495-496
Wagner, R., 657
wagtail: Motacilla, q.v.
Wald, 100, 375
Walker, C, 550
Walker, E., 230
wallabies (mammals: smaller macropodids)

color vision in, 518

habits of, 227, 518

pupils of, 227
walleye, wall-eyed 'pike': Stizostedion, q.v.
Walton, 510-511

walrus: Odobcenus (a pinniped, q.v.), pupil
warblers, eye size in, 641 [of, 447

Washburn, 473, 511
water

-balance of fishes, 370-373

deep, characteristics of, 393-395

properties of, 369-380, 462, 488-489

-surface, vision through, 377-379, 378

visibility through, 375-376

vision in (see aquatic, amphibious activity)
water-ouzel: dipper, q.v.
water-snakes (do not include river-snakes,

sea-snakes [^^.v.]; see also Na/rix)

accommodation and refraction in, 272-273
soft lenses and, 282-283, 438, 630
Watson, 484, 498, 508-511, 516
wavelength, units of, 4
Waugh, 510

weasel, color change in, 524
Weber, 537, 539; law of, 464, 534*535
weeping, psychic, 41
weever: Trachinus, q.v.
Weldon, 524
Wessely, 646, 651, 657
whales (mammals: order Cetacea)

accommodation and refraaion in, 272-273

biology of, 410-412

blue, size of eye in, 677

ciliary body, shape of, in, 286

ciliary processes in, 681

compared with crocodilians, 422

compared with sirenians, 408, 412, 422

deep swimming by, 209-210

eyes in, 412-417, 413

size of, 171, 415, 445, 677

fixation by, 310

habits of, 368-369, 410-417

iris in, 678

lashlessness of, 426

lens in, 445-446, 683

muscle of Mijller in, 272,, 285

necklessness of, 377

pupil in, 221

operculum of, 162, 219

retina in, 216

sclera in, thickness of, 415-417, 569

tapetum lucidum in, 233, 241

taxonomic position of, 139, 675

vision of, 210, 375-376
wheel, movement of, 352
whip-poor-will, eyeshine of, 646
whip-snakes: Masticophis {q.v.) et al;

yellow lenses of, 199
White, 483
white valence, 86*
Wilson, 541-542

Winslow, little stars of, 232*, 234
Winterid (deep-sea teleost), forward aim of

tubular eyes in, 402
Wojtusiak, 494-496
Wolf, 520
wolf (a canid carnivore)

habits, eye size, and tapetum lucidum of,

optic axes of, 297 [145

Wolff, 487

wolverine, tapetum lucidum of, 234
woodchuck: Marmota, q.v.
woodcock: a snipe, q.v.
woodpeckers (bird family Picidae)

chorioid in, 645-646

Gemminger's ossicle in, 643

oil-droplet colors of, 502
worm-lizards: burrowing, degenerate-eyed
lizards of the families Amphis-
bcenidcP, Euchirotids, Dibamidae,
Anelytropidffi (qq.v.)

California: Aniella, q.v.

eyes of, 458

habits of, 200

spectacles of, 450
worm-snakes: burrowing, degenerate-eyed

snakes of the families Typhlopida
Leptotyphlopidae (= Glauconiids ) ,
qq.v.; habits of, 201
Worth, 503

INDEX AND GLOSSARY

785

wrasses: Labrids, q.v.
Wunder, 61, 176, 236
Wundt, 321
Wychgram, 648

xantholeucophores, 526*, 595
xanthophores, 526*

xanthophyll: a carotenoid pigment, q.v.
Xantusia (reptile: night-lizard; see also
next entry)
ciliary muscle in, 624
conus papillaris in, 625
dermal color changes in, 541
pupil of, 220
trace of fovea in, 625
visual cells of, 62, 78, 168, 200, 203,
626-627
rhodopsin lacking in, 78
XantusiidcE (reptiles: a lizard family; see
also Xantusia)
ciliary muscle in, 624
contrasted with snakes, 634
habits of, 200, 458
loss of fovea by, 621
oil-droplets in, 200
possible color vision of, 520
pupil in, 220
spectacles of, 450
trace of fovea in, 625
Xenarthra (order of mammals; most 'eden-
tates' : sloths, armadillos, and ant-
bears)
optic axes of, 297
retina of

avascularity of, 684
lack (?) of cones in, 685
size of eye in, 677
taxonomic position of, 676
Xenopeltis (reptile: monotype of a snake
family intermediate between Boids
and Colubridse)
habits of, 201, 450
pupil of, 220
retina of, 636-637
spectacle of, 450
Xenopus (amphibian: dagger-frog)
dermal color changes in, 535

rhythmic, 538
lower lid of, 593
permanently aquatic habit of, 368

Xiphias (teleost: swordfish)
coloration and habits of, 526
scleral ossicles of, 271, 381

Yerkes, 484, 491, 510
Young, 524
Young, J. Z., 537-538
Young, T., 88-89

-Helmholtz theory of color vision, 75,
89*, 98, 101, 338, 513

Z.aglossus (mammal: an echidna), 663*;

ocular structure in, 664-671
Z.amenis (reptile: a colubrid snake),
binocular field of, 293-294
Z.aocys (reptile: a colubrid snake),

binocular field of, 294
Zapfensubstanz, 100*, 101-103, 495
zebra grass-parakeet, Australian:

Melopsittacus, q.v.
Zenion (deep-sea teleost), huge eye of,

395, 400,402
Zenkerella (mammal: a flightless anomal-
urid rodent)
diurnality of, 227
pupil of, 221
Zinn, zonule of (see zonule)
Ziphiidae mammals: beaked whales), 412
Zolotnitzky, 473, 480
zonule, 19*

as check-ligament, 268, 285, 683
development of, 115, 117

TAXONOMICALLY:

lampreys (lacking), 259

elasmobranchs, 260, 268, 372, 429, 564,

teleosts, 261 [567

amphibians, 266-267, 596, 602

chelonians, 609

Sphenodon, 618-619, 624

lizards, 624, 646

snakes, 628-631

birds, 645-646

monotremes, 667, 669

placentals, 681-683
man, 7, 19, 683
Zonurus (reptile: a zonurid lizard)

eye-movements of, 306

visual fields of, 294
Zygixna: Sphyrna, q.v.