!.?;':'iiiK,M ' ''■:;iH(Kiii»iMs;'.' lilllll SYSTEM OF OPHTHALMOLOGY The scheme for the "System of Ophthalmology" is as follows, but its division into different volumes is liable to alteration. Vol. I. THE EYE IN EVOLUTION Vol. II. THE ANATOMY OF THE VISUAL SYSTEM Vol. III. NORMAL AND ABNORMAL DEVELOPMENT Pt. I. Embryology Pt. II. Congenital Deformities Vol. IV. THE PHYSIOLOGY OF THE EYE AND OF VISION Vol. V. OPHTHALMIC OPTICS AND REFRACTION Vol. VI. OCULAR MOTILITY AND STRABISMUS Vol. VII. THE FOUNDATIONS OF OPHTHALMOLOGY Heredity, Pathology, Methods of Diagnosis, General Therapeutics Vol. VIII. DISEASES OF THE OUTER EYE Pt. I. Conjunctiva Pt. II. Cornea and Sclera Vol. IX. DISEASES OF THE UVEAL TRACT Vol. X. DISEASES OF THE RETINA Vol. XL DISEASES OF THE LENS AND VITREOUS; GLAUCOMA AND HYPOTONY Vol. XII. NEURO-OPHTHALMOLOGY Vol. XIII. THE OCULAR ADNEXAn Lids, Lacrimal Apparatus, Orbit and Para- orbital Structures Vol. XIV. INJURIES Vol. XV. INDEX OF GENERAL AND SYSTEMIC OPHTHALMOLOGY SYSTEM OF OPHTHALMOLOGY EDITED BY SIR STEWART DUKE-ELDER G.C.V.O., M.A., LL.D., Ph.D., D.Sc, M.D., D.M., F.R.C.S., F.R.C.S.E., F.A.C.S., F.R.A.C.S. VOL. I THE EYE IN EVOLUTION BY SIR STEWART DUKE-ELDER WITH 902 ILLUSTRATIONS, 15 COLOURED PLATES AXD 3.')0 MARGINAL ILLUSTRATIONS ST. LOUIS THE C. V. MOSBY COMPANY 1958 @1958 by Henry Kimpton Publishers, 7 Leighton Place, Leighton Road, London NWH All rights reserved. No part of this publication may be reproduced, stored in a retrieval system, or trans- mitted, in any form or by any means, electronic, mechanical, photocopying, recording or otherwise, without the prior permission of the publishers. Reprinted 1970, 1976 ISBN 0 85313 213 a MADE AND PRINTED IN GREAT BRITAIN PREFACE The reception accorded to my Textbook of Ophthalmology has per- suaded me that there is a need for its continuation in a second edition. The seven volumes of the Textbook took almost a quarter of a century to write, a period unfortunately longer than it might have been owing to the exigencies of war. The first four volumes have long been out of print — and inten- tionally so because they have long been out of date. It is to be remembered that the second volume was written before the suljjhonamides were intro- duced ; the third before the antibiotics revolutionized the therapeutics of infective diseases ; both of them before the role of viruses in ocular disease was adequately appreciated ; the physiology of the eye of yesterday is unrecognizable when compared with that of today ; even the anatomy has been transformed by more elaborate optical and chemical methods of investigation and the advent of the electron microscope. The re-writing of the whole work if its com^^rehensive nature were to be retained would be an immense task occupying more time than I could reasonably expect to have at my disposal. Moreover, tomorrow ^^•ill be different from today, and if a work such as this is to be of any lasting value it would seem to me desirable that a new edition be published at least every fifteen or twenty years ; fortunately, ophthalmology is no static science. It therefore seemed to me wise to sliare the task of re-writing the original Textbook with my colleagues at the Institute of Ophthalmology in London. I am grateful that they have accepted this burden. For this reason I have changed the name of the book to a ''System of Ophthalmology " since it will necessarih^ be less personal. This first volume in the new series is an extension of the first twenty pages of Volume I of the old Textbook ; this I have %^Titten myself, largely because it is a subject in which I am particularly interested — and I wished to write it. The subject-matter has never been gathered together in a single book before and it is my hope that it will interest ophthalmologists in so far as it forms the basis of the science of vision ; and it may be that it will be of value also to those whose interest is biological rather than clinical. ; The numerous marginal sketches are not usual in a book of this type. To the student of natural history they may seem superfluous, but to the ophthalmologist some of the animals may be unfamiliar and the drawings may perchance add meaning to the zoological nomenclature and thus give the text more life and interest. It is to be noted, however, that they are drawn not to scale, but approximately to a standard size to fit into a 1-inch margin, Stewart Duke-Elder. Institute of Ophthalmology, London, 1957. ACKNOWLEDGEMENTS In the preparation of this book I have incurred a considerable amount of indebtedness which is a pleasure to record. Many of the illustrations are borrowed, and in each the source is acknowledged. There are, however, five sovirces from which I have liberally drawn, and these merit special thanks : Dr. Gordon Walls, for a number of his original drawings ; Masson et Cie of Paris, who have allowed me to use some illustrations from Rochon-Duvigneaud's classical work, Les Yeux et la Vision des Vertebris ; Dr. Maurice Burton and his publishers, the Elsevier Publishing Co. of Holland, for some illustrations from The Story of Animal Life ; the Royal Society for permission to iise a large number of Lindsay Johnson's illustrations published in their Proceedings ; and Macmillan & Co. for giving free permission to copy a large number of the illustrations of animals in the Cambridge Natural History in the form of inarginal sketches. In preparing the illustrations I have had the willing co-operation of Dr. Peter Hansen and the Department of Medical Illustration of the Institute of Ophthalmology, the assistance of which, particularly that of Mr. T. R. Tarrant, the Medical Artist, has been invaluable. The Zoological Society of London has lent me a number of photo- graphs, as also has the Natural History Museum of London, together with specimens of various invertebrates. Professor Ida Mann has allowed me to use a large number of her illustrations of the eyes of animals, and Dr. Kevin O'Day of Melbourne has allowed me to use photographs and slides of the eyes of Monotremes and Marsupials which are unobtainable outside Australia ; while in this Institute Professor Norman Ashton and Dr. Katharine Tansley have provided me with sections and photographs of the eyes of a number of animals. In several instances my knowledge of zoology has been brought up to date by the great kindness of Dr. Mary Whitear of the Zoology Department of University College, London, who has read the proofs of those sections dealing with zoological classification ; while Dr. Katharine Tansley and Dr. Robert Weale of this Institute have given me most helpful criticism in some aspects of the visual problems discussed. Miss M. H. T. Yuille, Mr. A. J. B. Goldsmith and my wife have shared with me the onerous task of proof-reading. It is difficult for me to express my indebtedness to my secretary. Miss Rosamund Soley, who has borne much of the burden of the technical aspects of the production of this Volume. She has typed and iDrejDared the manuscript, corrected the proofs, and undertaken the immense and somewhat thankless task of verifying the bibliographies, prepared the Zoological Glossary and the Index, and drawn the 350 marginal sketches. Finally, my indebtedness to my publishei's, Henry Kimpton, continues to be immense. They have assisted me in every possible way. Why Mr. G. E. Deed con- tinues to put up with my inoods and vagaries after thirty years is to me quite incomprehensible. Stewart Duke -Elder. CONTENTS VOLUME I THE EYE IN EVOLUTION Part I. The Effect of Light on Living Organisms Chapter I Introduction The Scope of the Subject The Responses of Organisms to Light Photosynthesis Chapter II The Effect of Light on Metabolism : Photoperiodism MetaboHc Effects of Light . Photoperiodism in Plants Photoperiodism in Animals . (a) Metabolic Activities . (b) Sexual Cycle of Animals (c) Pigment Migration . (d) Bioluminescence (e) Time -memory of Insects and Birds 7 9 13 13 16 19 21 22 Chapter III The Effect of Light on Movement Historical Development Types of Motorial Responses (a) Photokinesis (i) Orthokinesis (ii) Klinokinesis (b) Phototropism . (c) Phototaxis (i) (ii) (iii) (iv) (V) (vi) Klinotaxis Tropotaxis Telotaxis Scototaxis Menotaxis Light-compass Reaction, 61 ; Navigational Sense in Birds, 63 ; Orientation to Polarized Light, 66 ; Orientation of Insects Out-of-doors, 67 ; Orientation to a Visual Pat- tern, 73 ; Dorsal (Ventral) Light Reaction, 74 Mnemotaxis ......... 27 31 33 34 34 38 42 47 52 55 60 60 78 CONTENTS Chapter IV The Effect of Light on Pigmentation The Types of Colour Change Mechanism of Colour Changes Chromatophores . Types of Pigment Types of Response Primary, 89 ; Secondary, 91 ; Indirect, 92 Central Organization of Pigmentary Changes, Nervous and Hormonal Chapter V The Emergence of Vision Light -sensitiveness, the Light Sense and Vision .... PAGE 82 85 85 87 89 92 102 Part II. The Evolution o! the Visual Apparatus Chapter VI The Morphology of Invertebrate Eyes I. The Genesis of the Eye .... Dermal Photosensitivity. Specific Light-sensitive Cells . Pigments ..... Melanin, 118 ; Visual Pigments, 118 Ommochromes, 122 II. The Structure of Invertebrate Eyes 1. Eye-spots : Stigmata 2. Light-sensitive Cells . 3. The Simple Eye (a) The Unicellular Eye . (6) The Multicellular Simple Eye (i) The Subepithelial Eye (ii) The Epithelial Invaginated Eye The Flat Eye, 136; the Cupulate Eye, 137; the Vesicular Eye, 141 (iii) The Inverted Retina (c) Aggregate Eyes ..... (d) Composite Ocelli ..... 4. The Compound Eye ...... (a) The Development of Ocelli and Compound Eyes (6) The Structure of the Compound Eye . The Simple Ommatidial Eye, 159 ; the Composite Com pound Eye, 160 (i) The Compound Eyes of Arachnids (ii) The Compound Eyes of Crustaceans (iii) The Compound Eyes of Insects (c) The Optical System of the Compound Eye The Appositional Eye, 173 ; the Superpositional Eye, 174 ; the Analysis of Polarized Light, 174 113 114 115 117 126 125 127 129 130 132 132 135 146 151 152 154 156 157 160 163 166 170 CONTENTS XI Chapteb VII The Systematic Anatomy of Invertebrate Eyes The Structural Variability of Invertebrate Eyes I. Protozoa .... II. Parazoa (Porifera : Sponges) III. Invertebrate Metazoa . 1. Coelenterata (a) Cnidaria . Hydrozoa ; Scyphozoa ; Anthozoa (b) Acnidaria : Ctenophora 2. Echinodermata ..... Holothuroidea, 184 ; Echinoidea, 185 ; Asteroidea, 185 3. Worms .... (a) Unsegmented Worms (i) Platyhelminthes Turbellaria, 188 ; Trematoda, 189 ; Cestoda, 189 (ii) Nemertea (iii) Nematoda (6) Segmented Worms : Annelida (i) Oligochpeta . (ii) Polycheeta (iii) Archiannelida (iv) Hirudinea : Leeches 4. Chgetognatha : Arrow-worms 6. Rotifera . 6. Polyzoa : Bryozoa 7. Brachiopoda : Lamp Shells 8. Mollusca ... (a) Placophora (b) Solenogastres . (c) Seaphopoda (d) Gastropoda (e) Lamellibranchiata (/) Cephalopoda 9. Arthropoda (a) Onychophora . Crustacea . Myriapoda Arachnida Scorpionidea, 211 ; Xiphosura, 212 ; Araneida, 213 Pseudoscorpionidea, 214 ; Pedipalpi, 214 ; Phalangida 215 ; Solifugae, 216 ; Acarina, 216 ; Pycnogonida, 21' Insecta ....... (i) The Stemmata of Larval or Pupal Forms (ii) The Dorsal Ocelli of Adults . (iii) The Compound Eyes of Adults (b) (c) (d) {e) PAGE 178 180 181 181 181 182 182 182 183 186 187 188 189 190 190 190 191 193 193 194 194 194 195 195 196 197 197 197 200 201 204 204 206 210 211 217 222 224 224 Chapter VIII The Eyes of Proto-chordates 1. Hemichordata ....... 2. Tunicata : Urochordata ...... 3. Cephalochordata : Lancelots ..... 227 228 228 Xll CONTENTS Chapter IX The Evolution of the Vertebrate Eye The Vertebrate Phylum ..... 1 . The Phylogeny of the Vertebrate Eye 2. The Ontogeny of the Vertebrate Eye 3. The Emergence of the Vertebrate Eye 4. The General Structm-e of the Vertebrate Eye PAGE 233 237 239 242 248 Chapter X The Eyes of Cyclostomes The Class of Cyclostomes 1. The Ammoccete Eye Light-sensitive Cells 2. The Lamprey Eye . 259 261 263 263 Chapter XI The Eyes of Fishes General Configviration of the Eye . The Class of Fishes L The Selachian Eye . 2. The Holocephalian Eye 3. The Teleostean Eye 4. The Dipnoan Eye 5. The Coelacanth Eye 6. The Chondrostean Eye 7. The Holostean Eye Anomalies in the Eyes of Fishes (a) The Tubular (Telescopic) Eye (6) The Amphibious Eye (c) Stalked Eyes . (d) The Migratory Eye . 273 278 279 290 291 312 314 315 321 322 322 324 326 328 Chapter XII The Eyes of Amphibians The Class of Amphibians General Configuration of the Eye. 1. The Anuran Eye 2. The Urodelan Eye . 333 334 334 346 Chapter XIII The Eyes of Reptiles The Class of Reptiles . General Configuration of the Eye 1. The Lacertilian Eye 2. The Chelonian Eye . 3. The Crocodilian Eye 4. The Rhynchocephalian Eye 5. The Ophidian V.ye . 353 353 355 368 375 379 383 CONTENTS Xlll Chapter XIV The Eyes of Birds The Class of Birds General Configuration of the Eye. The Avian Eye 397 401 401 Chapter XV The Eyes of ]\Iam>iaxs The Class of Mammals 1. The Monotreme Eye 2. The Marsupial Eye . The Sub-class of Placentals 3. The Placental Eye . Aquatic Adaptations 429 431 437 441 446 501 Chapter XVI The Central Organization of Vision General Principles II. The Nervous Control 1. The Nerve -net 2. Trunk-pathways 3. The Ganglionic Nervous System (a) The Nervous System of Worms (6) The Nervous System of Arthropods . (c) The Nervous System of Molluscs 4. The Central Nervous System of Vertebrates Hind-brain, 533 ; Mid-brain, 534 ; Diencephalon, 537 mus, 538 ; Telencephalon, 542 Evolution of the Visual Pathways and Centres The Hormonal Control ...... Hormones and Neuro -secretory Cells (a) The Neuro-endocrme System of Crustaceans (b) The Neuro -endocrine System of Insects (c) The Neuro -endocrine System of Vertebrates Optic Thala- 509 511 614 616 617 518 521 527 530 543 647 550 552 555 556 Part III. The Function of the Eyes of Animals Chapter XVII The Vision of Invertebrates Methods of Investigation ..... 1. The Reactions of the Lower Invertebrates to Light (a) Protozoa ..... (b) Coelenterata ..... (c) Echinodermata .... 567 670 570 571 571 XIV CONTENTS 2. The Vision of Worms .... (a) Unsegmented Worms (6) Segmented Worms 3. The Vision of Molluscs .... (a) Gastropods and Lamellibranchs (6) Cephalopods 4. The Vision of Arthropods (a) Onychophora (6) Myriapods (c) Crustaceans (d) Arachnids 5. The Vision of Insects (a) The Larvse of Insects .... (b) The Dorsal Ocelli of Adults . (c) The Compound Eyes of Insects (i) Behavioural Experiments (ii) Electro-physiological Characteristics (iii) Spectral Sensitivity (iv) Discrimination of Luminosity-differences (v) Perception of Colour . (vi) Perception of Form . (vii) Perception of Distance (viii) Spatial Appreciation and Localization Accommodation in Invertebrates PAGE 572 572 572 574 574 575 677 578 578 578 579 681 582 582 683 583 584 584 585 586 588 589 589 590 Chapter XVIII The Vision of Vertebrates The Role of Vision in Vertebrate Life (a) Cyclostomes (b) Fishes (c) Amphibians {d) Reptiles (e) Birds (/) Mammals I. The Perception of Light 1. The Nocturnal Eye (a) The Optical System The Tapetum Lucidum (b) The Organization of the Retina 2. The Diurnal Eye .... 3. The Arhythmic Eye (a) Contractile Pupils (6) Occlusible Tapeta . (c) Photo -mechanical Changes in the Retina (rf) The Static Organization of the Retina 4. Absolute Sensitivity to Light . 6. Discriminati of Variations in Intensity . 597 598 698 599 599 600 600 602 605 605 606 609 611 612 612 612 614 616 616 617 CONTENTS XV PAGE II. The Perception of Colour ......... 619 Objective Methods of Investigation ...... 621 Subjective Methods of Investigation ...... 623 1. The Colour Vision of Cyclostomes ....... 624 2. The Colour Vision of Fishes 624 3. The Colour Vision of Amphibians ....... 627 4. The Colour Vision of Reptiles ....... 628 6, The Colour Vision of Birds 629 6. The Colour Vision of Mammals ....... 632 III. The Perception of Form ......... 637 1. Optical Factors 638 (a) The Refraction of Vertebrates ...... 638 (6) Accommodation in Vertebrates ...... 640 (i) Static Devices ........ 640 Stenopoeic Pupil, 641 ; Duplicated Optical System, 641 ; Interposition of Nictitating Membrane, 643 ; Duplicated Retina, 643 ; Ramp-retina, 643 ; Cor- rugated Retina, 643 ; Length of Receptor Elements, 643 (ii) DjTiamic Devices ....... 644 (a) Movement of Lens as a ^^^^ole .... 644 Backward Movement, 644 ; Forward Movement, 647 (^) Deformation of Lens ...... 649 By Direct Ciliary Pressure, 649 ; by Capsular Elasticity, 652 (iii) Accommodation in Amphibious Vertebrates . . . 654 (c) Other Optical Factors determining Visual Acuity . . . 655 2. The Structure of the Retina 656 (a) The Area Centralis ........ 657 (b) The Fovea 658 (c) The Degree of Summation ....... 659 3. The Visual Acuity of Vertebrates ....... 660 (a) The Visual Acuity of Fishes 660 (b) The Visual Acuity of Amphibians . . . . . .661 (c) The Visual Acuity of Reptiles . ...... 661 (d) The Visual Acuity of Birds 662 (e) The Visual Acuity of Mammals ...... 663 rV. The Perception of Space 1. The Visual Fields of Vertebrates (a) The Uniocular Field (6) The Binocular Field Cyclostomes, 678 ; Fishes, 678 682 ; Birds, 684 ; Mammals, 2. The Ocular Movements . (a) Involuntary Ocular Movements (6) Voluntary Ocular Movements Fishes, 693 ; Amphibians, 694 Mammals, 696 Amphibians, 682 687 Reptiles, 666 669 669 672 689 690 692 Reptiles, 694 ; Birds, 695 XVI CONTENTS The Perception of Space — contd. page 3. Uniocular and Binocular Vision ....... 697 Spatial Judgments . . . . . . . . .700 Fishes, 701 ; Amphibians and Reptiles, 702 ; Birds, 702 ; Manmials, 704 V. The Perception of Movement . . . . . . . .705 Part IV. Evolutionary By-ways Chapter XIX Median Eyes 1. Pineal and Parietal Organs . . . . . . . .. 711 Cyclostomes, 713 ; Fishes, 713 ; Amphibians, 714 ; Reptiles, 715 (a) The Median Eye of the Lamprey . . . . . .716 (6) The Median Eyes of Lizards and /S^/ienorfon . . . . .716 2. The Function of the Pineal and Parietal Organs . . . . .718 Chapter XX Rudimentary Eyes Habit and Regression . . . . . . . . . .721 1. The Sedentary Habit 722 Molluscs, 722 ; Crustaceans, 722 2. The Abyssal Habit 722 Molluscs, 723 ; Crustaceans, 723 ; Fishes, 723 3. The Cavernicolous or Limicoline Habit . . . . . .724 Invertebrates, 724 ; Cave-fishes, 725 ; Amphibians, 726 4. The Fossorial or Burrowing Habit . . . . . . .728 Invertebrates, 728 ; Amphibians, 730 ; Reptiles, 731 ; Mammals, 733 5. The Parasitic Habit 733 Invertebrates, 733 ; Cyclostomes, 734 ; Fishes, 734 Chapter XXI Luminous Organs Bioluminescence ..... 1. The Occurrence of Bioluminescence . The Biological Purpose of Bioluminescence 2. The Biological Mechanism of Bioluminescence Extracellular Bioluminescence Intracellular Production of Bioluminescence 3. The Chemical Mechanism of Bioluminescence 736 737 741 744 745 746 747 Chapter XXII Electric Organs The Electric Organs of Fishes : Astroscopus EPILOGUE APPENDIX. Pala^ontological Table . Zoological Glossary .... Index ...... 751 753 754 756 779 PART I THE EFFECT OF LIGHT ON LIVING ORGANISMS Introduction The Effect of Light on Metabolism The Effect of Light on Movement The Effect of Light on Pigmentation The Emergence of Vision S.O.— VOL. I. Fig. 1.— Charles Darwin (1809-1882). (From a portrait by John Collier in the Linnean Society.) CHAPTER I INTRODUCTION We begin with a drop of viscid protoplasm the reactions of which we do not understand, and we end lost in the delicacy of the structure of the eye and the intricacies of the ten thousand million cells of the human brain. We begin with photosjnithesis in a unicellular plant, or with a change in the viscosity produced by light in the outer layers of the amoeba, and we end with the mystery of human perception. We begin some one or two thousand million years ago in the warm waters of the Archeozoic era and we end with the speculations of tomorrow. And as we travel together tracing the responses of living things to light from the energy liberated by a simple photochemical reaction to the faculty of appreciating and interpreting complex perceptual patterns, neither in fact nor in fiction does a story more fascinating unfold. It is a story which traces a development from a vague sentiency to apperception, from vegetative existence to the acquisition of the power to mould the environment, from passive reactivity to the ability to create history. Nor is there a story more important. Even at the physiological level some 38% of our sensory input is derived from the retinae,^ impulses from which, even in the complete absence of visual stimuli, are largely responsible for maintaining a tonic influence upon the level of spontaneous activity in the brain. ^ From the psychological point of view the importance of vision is still greater. If, indeed, the proper study of mankind is Man, and if (as we must agree) his behaviour and his contact with the outside world are mediated through his senses, what can be more fundamental than the study of the sense which, more than any other, determines his intelligence and regulates his conduct, of the faculty which eventually played the preponderant role in assuring his dominance and determining his physical dexterity and intellectual supremacy ? We are indeed highly visual creatures. It would seem appropriate to introduce a book devoted to the evolution of vision with a portrait of charles darwin (1809-1882) (Fig. 1), the great English naturalist who, like Newton in the world of physics, was one of the very few men who revolutionized world thought in the subject on which he worked— and beyond. But Darwin has a special claim to introduce this chapter, for at a time when the conduct of animals was generally ascribed to the existence of vital forces or psychic activities, and when the orientation of plants was thought to be due to the direct influence of physical stimuli such as light and heat upon the ^ According to the calculations of Bruesch and Arey (J. cx>mp. Neurol., 77, 631, 1942). 2 See Claes [Arch, intern. Physiol., 48, 181, 1939) and many others, admirably summarized in Grauit {Receptors and Sensory Perception, New Haven, 1955). 3 THE EYE IN EVOLUTION plant as a whole, he transformed biology to a more factvial plane based on observation and experiment, and was the first to show that in the higher plants receptor tissues existed separately from motor tissues, and that the orientation of plants to light was due to the transference over some distance of stimuli appreciated by the former to be made effective by the latter. These observations which appeared in the last of the classical books derived from his pen ^ form a typical example of the revolutionary nature of Darwin's philosophy — the result of a unique combination of experimental genius with penetrative powers of interpretation which have rarely been equalled — and from these observations have directly followed our understanding of the development of the sensory organs and their effect on the evolution of the higher species in the animal scale. The son of a doctor in the English country town of Shrewsbury, he went to the University of Edinburgh to study medicine ; this, however, he forsook and went to Cambridge with the intention of entering the Church ; but here Sedgwick and Henslow, the professors of geology and botany, inspired him again with a love of natural history which eventually was to become a passion. Darwin's assessment of the qualities responsible for his own success is worth remembering : " the love of science, unbounded patience in long reflecting over any subject, industry in observing and collecting facts and a fair share of invention as well as of common sense ". And again : "I have steadily endeavoured to keep my mind free so as to give vip any hypothesis, however much beloved (and I cannot resist foi-ming one on every subject), as soon as facts are shown to be opposed to it ".- THE RESPONSES OF ORGANISMS TO LIGHT LIGHT — the visible radiant energy derived from the sun — is respon- sible for the whole existence of living things on the earth, and without question photosynthesis in plants — the reaction whereby the carbon dioxide and water which permeate the atmosphere and the earth's crust are converted into the organic substances which constitute the basis of all living things — is the most fundamental and important chemical process on our planet. Not only was photosynthesis respon- sible for the origin of 'life but it maintains the perpetual cycle of the activities of living things. By oxidation, living structures are con- tinuously broken down to their initial constituents (carbon dioxide and water), the process being accompanied by the liberation of the energy required by organisms to perform their varied activities ; by photosynthesis the carbon dioxide and water produced by the oxidation of living matter are perpetually reunited by an opposite process of reduction with the return of oxygen to the atmosphere, the high energy requirements necessary being supplied by the capacity of the chloro- phyll group of pigments in green plants to absorb sunlight. This reaction whereby the chlorophyll system stores and then liberates light-energy is thus not only the source of the activities of all living things but supplies much of the energy at the disposal of the civilized world in the stores of coal and petroleum formed throughout the ages. ^ Pouer of Movements in Plants, London, 1880. ^ Life and Letters of Darwin, by Francis Darwin, 1887. RESPONSES OF ORGANISMS TO LIGHT It would be out of place to enter fully into the mechanism of photosynthesis by chlorophyll here ; for a recent summary the reader is referred to the mono- graph by Hill and Whittingham.i The chlorophyll group of pigments are tetra- pyrrolic compounds in which magnesium is present in non-ionic form ; they are related to hgemin which, however, contains a central iron atom. The completed process whereby carbohydrates are synthesized has long been known and may be represented by the equation : .rCOj + .rHaO + radiant energy -^ Ca;H2j;0a; + .rOj + stored energy. The intimate mechanism, however, has only recently begun to be analysed, an advance largely due to the use of radio-active carbon (i*C) as a " tracer ". Although many of the details are still obscure, particularly the way in which chlorophyll absorbs radiant energy and directs it into chemical processes, the basic reactions are known and can indeed be carried out in the test-tube. The essential process is the photolysis of water. Chlorophyll induces the energy derived from light to break the hydrogen-oxygen bonds in the molecule of water ; the hydrogen therefrom is used to convert the single carbon atoms of CO 2 into long-chained carbohydrates through the medium of phosphoglyceric acid and the oxygen is liberated as a free gas ; meantime a store of chemical energy is provided by the photosynthesis of energy-rich compounds such as adenosine triphosphate, the break-down of which by simple hydrolysis releases large amounts of energy to drive the process. It is probable that these and the many other compounds fovind in jjlants are formed by enzyme-reactions from one or more of the constituents of the photosynthetic cycle at either the C3 or Cg level. ^ Apart from this basic activity which characterizes the vegetable world, light produces photochemical reactions of great variety in living organisms. The energy thus liberated produces in the most primitive creatures the only response available — a change of general activity, frequently of motion, just as do other stimuli, mechanical, gravitational, thermal, chemical or electrical ; in the higher forms a multitude of activities may be initiated or influenced. These responses we will review under four main headings. In the first place, the response may take the form of a change in general metabolic activity, usually, but not invariably, an increase of activity under the influence of light. As a natural extension of this, the diurnal cycle of light and darkness has in the course of evolution so impressed itself upon a number of the fundamental activities of many organisms (including man) that these show a corresponding rhythm which has eventually become innate and endogenous (photoperiodism). In the second place, the response may be expressed as a variation in movement. In its simplest form this is also merely a change in general activity wherein movements are random in nature and undirected (photo - kinesis) ; as an evolutionary extension of this the movements initiated by light come under the directional control of the stimulus so that the organism is orientated by light in a definite way ; such movements 1 Photosynt}(e.sis. London, 1955. See also Proc. roy. Soc. B, 157, 291 (1963). 2 For reviews, see Arnon (An?i. Rev. plant Physiol.. 7, 325, 1956, Nature (Lond.), 184, 10, 1959), Rosenberg (Ibid., 8, 1957). THE EYE IN EVOLUTION may affect the component parts of sessile organisms (phototropism) or may be expressed in translatory movements by motile organisms (phototaxes). In the third place, light acting directly or indirectly is the most potent stimulus for altering the pigmentary distribution in both plants and animals — an understandable reaction since pigment has been evolved specifically for the absorption of light, either to utiHze its energy or as a protection against its excess. All these activities have become more complex as evolution has proceeded. The most primitive required no specific organization ; the more complex called for the acquisition of one or more receptor organs, which in their most elementary stages need appreciate only changes in the intensity of the light, but in their more advanced forms must analyse the direction of its incidence and its spatial distribution. Initially, in some unicellular organisms a diffuse reactivity sufficed ; but as multicellular organisms developed, the stimulus must needs be transported to the effector organs, either chemically by hormones or by nervous activity. In this way the effects of light upon metabolism, orientation and pigmentation became correlated through primitive nerve-nets and then became integrated in the ganglia of the central nervous system ; and eventually, when the nervous pathways from the eyes were projected into a head-ganglion and ultimately into the fore- brain, the highly complex faculties of vision and apperception evolved. CHAPTER II THE EFFECT OF LIGHT ON METABOLISM It is well known and iniiversally recognized that the general behaviour of many organisms is regulated by light ; the contrast between the activities of nature by day and its stillness by night needs no stress. This is a widespread characteristic of vegetable life which exists so much more closely to the sun and the earth than do animals, but even among the latter dramatic changes are frequently evident, particularly in the lower forms. Thus among Protozoa, some Rhizopods change their form, contracting under the influence of light (Engelmann, 1882 ; Verworn, 1889) (Figs. 2 and 3), many species are activated by light (such as flat-worms, Loeb, 1893-94), while other creatures become inactive under its influence (maggots, Herms, 1911 ; and many insects, such as cockroaches, Gumi, 1940). Among the higher forms of life, in addition to a number of basic metabolic functions, the reproductive Fig. 2. Fig. 3. Figs. 2 and 3. — Pelomyxa pahistris at rest (Fig. 2), and contracted under the influence of light (Fig. 3). cycle and secondary features such as colour changes and behavioural habits are similarly regulated by light although in many cases other factors such as temperature, humidity and nutrition exert sometimes contributory, sometimes more potent effects. In this way the alterna- tion of day and night has imposed a rhythmic diurnal cycle upon a number of the activities of living organisms (photoperiodism) ; and it is to be remembered that in many of the phenomena thus involved darkness seems to be as important a stimulus as light. Indeed, in many cases the rhythm has become so fundamental that if the organism is placed in experimental circumstances wherein the natural alternation of light and darkness is changed to become out-of-phase, or if it is exposed to continuous light or darkness, many of these cyclic changes continue as if the normal 24-hour rhythm still persisted ; the rhythm originally imposed by external circumstances has eventually become autochthonous. THE EYE IN EVOLUTION Fig. 4.— Carl Linn.t^us (1707-1778). Carl Linnsous, son of a Lutheran Swedish pastor and Professor of Botany at Uppsala, is universally acknowledged as the Father of Scientific Botany. His main work was his System of Nature which passed through 1 2 editions in his lifetime following its initial publication in 1741. He had a passion for classification. Not only did he classify in a system based on their reproductive organs the 18,000 species of plants known to him, which he and his pupils travelled far and wide to collect (one of them, for example, accompanied Captain Cook on his first voyage, 1768-71) ; but he also classified animals, diseases and minerals — even past and jiresent scientists in a system of military rank with himself as general. He introduced the now universally adopted nomenclature of plants and animals, first the generic name indicating the genus, and second the specific name indicating the species. His garden is still tended in Uppsala. The Linnean Society of London which jDOSsesses his library and collections was founded in 1788. This portrait of " Carl v. Linne astat. 67", lent me by the Linnean Society, is from the original by Krafft, the Swedish artist, who painted it in 1774 for the College of Physicians at Stockholm of which Linnaeus was one of the founders. LIGHT AND METABOLISM The origin of such rhythms is speculative, but it is interesting to recall the environment of living creatures when first they experienced the drama of a day- night cycle on the earth. For millions of years living organisms never experienced conditions more varied than those of the warm but placid sea, but as the sea- weeds of the swamps spread onto the land, plants became exposed alternately to the stimulating conditions of a humid hot-house during the day and the depression of the comjDarative chill of night. Similarly, as Amphibians emerged to creep upon the land in the heat of the Palfeozoic, and as thej' and the Reptiles matured in the torrid Jurassic and Cretaceous ages, it is difficult to realize the violence of the contrast between the extreme metabolic and nervous activity which must have occurred in the blaze of noon, and the sluggishness of sleep and the reduction of nervous energy which must have prevailed in the cold of night ; for chemical activity and the speed of nervous impulses are both dependent on temperature. It is probable, indeed, that the development of thermostasis and its ultimate evolution into homeostasis were the determining events which made possible the evolution and ultimate supremacy of Birds and Mammals on a cooling globe, and that the lack of the control of temperature was the main cause of the extinction of the Dinosaurs and the retreat of the Amphibians to a few degenerate types. But it is to be remembered that the period during which the primitive creatures which first inhabited the still-warm earth experienced this alternating climax of delirious activity each noon and fatigued torpidity each night, occupied some hundred million years ; and even although their descendants have long acquired the peace of thermostas's, it is not surprising that traces of the early turmoil still remain. PHOTOPEEIODISM IN PLANTS Over 200 years ago, carl linn.^us (1707-1778) (Fig. 4), who laid the groundwork of scientific botany at Uppsala, noted that many Figs. 5 and 6. — Sleep ^Movements in Flowers and Leaves. Fig. 5. — Oxalis rosea awake. Fig. 6. — Oxalis rosea asleep. 10 THE EYE IN EVOLUTION flowers have a time of opening and closing so regular that he constructed a flower-clock from which the time of day could be read — the poppy opened at 6 a.m., the speedwell at mid-morning, the white campion in the evening (to be pollinated by night moths), and so on (Figs. 5 and 6). At a much later date, the " sleep movements " of leaves were similarly studied by Darwin (1880) : those of the runner bean, for example, raise themselves during the morning, become horizontal by noon, fall in the afternoon and fold up at night. The significance of these daily rhythms, however, was largely neglected until they were intensively investigated by the German botanist, E. Blinning (1931-56), who showed that they were not simply an immediate response to the passing stimuli of day and night, but were part of a rhythmic change which has become characteristic and endogenous to the plant itself — a 24-hour rhythm in the intensity of endosmosis throughout its structure, in the rate of growth, the rate of respiration, the activity of enzymes and the entire metabolism, a rhythm to which the plant has become habituated so that the periodicity persists for some time even if it is placed in continuous darkness, and is only slowly readjusted if an artificial rhythm is imposed upon it.^. Other factors may supervene, the most important of which are temperature and nourishment, but the most profound influence on basic activities is that of the sun, from the energy of which all life is ultimately derived. The pattern of the flowering of many plants is a good example of this general tendency^ — and an important one, for floral initiation is a fundamental factor marking the change from vegetative life to reproduc- tive activity. Although experimental work of considerable merit had been done on the effects of artificially varying the periods of illumina- tion on the growth and maturation of plants, particularly by Schiibeler (1880) in England, Tournois (1912) in France, and Klebs (1918) in Germany,^ it was left to two American botanists. Garner and Allard (1920), to establish finally the important fact that in many species flowering did not depend primarily on temperature or the intensity of illumination but on the daily lengths of the periods of light and darkness ; they therefore introduced the term photoperiodism. In many plants the determining factor is the length of the day, and, as was first proved by the Russian botanist, Cailahian (1936), the primary receptor organ is the leaf ; even although the rest of the plant is covered, the exposure of one leaf, or even part of a leaf, to the rhythm of light and darkness determines the cycle, and if the leaves are removed and the plant rendered naked to live on its stored food it immediately becomes 1 See Grossenbacher (1939), Engel and Heimann (1949), Flligel (1949), Hagan (1949), Heimann (1950-52), Enderle (1951), Vegis (1955), Biinning (1956), Wareing (1956), and others. " For review, see Smith, 1933. LIGHT AND METABOLISM indifferent to the alternating change between darkness and light. Moreover, if a plant of one tyjDe is denuded of leaves and the leaf of a plant with a different cyclic character is grafted onto it, the host-plant assumes the periodicity of the grafted leaf.^ Two different responses are well recognized. In summer-flowering plants {long-day plants) which bloom when the spring days lengthen, the formation of 11 Fig. 7. — The Effect on Flowerixg of Ixtermittent Light during the Night. On the /eft are two gladioli (long-day plants) grown in a control green- house with a normal solar day-and-night rhythm ; on the right, two similar plants growai with intermittent light during the night (Boyce Thompson Institute for Plant Research). flowers is inhibited in darkness while during the periods of light some substance is presumably formed in the leaves which counteracts this inhibition ; in short- day plants which come to flower when the autumn days shorten, both dark and light periods are necessary for the develoiament of the stimulus, each with opposite effects, one depending on light-energy and the other being inhibited by light. In summer-flowering jolants artificial light during the night promotes flowering (Fig. 7) ; in autumn-flowering plants flowering in short days, light during the day promotes flowering but short joeriods of light during the night prevent it. 1 Melchers (1936-37), Cailahian (1936-47), Loehwing (1938), Borthwick and Parker (1938-40), Hamner and Naylor (1939), Harder and v. Witsch (1940), Withrow et al. (1943), and others. 12 THE EYE IN EVOLUTION The mechanism of these photoperiodic responses is unknown but several facts are now estabhshed. It is significant that a brief exposure (1 sec. in some species) to fight of a very low intensity (of the order of 1 ft. candle, that is, of the intensity of moonlight) is sufficient to determine the periodicity. The wave-length of the fight is of import- ance, for the action-spectrum shows a specificity with maxima in the red and blue — a fact which suggests the presence of one or more absorbing pigments ; moreover, there are indications of an antagonism between the action of different spectral regions, while near infra-red radiation takes an active part in the effect (see Wassink and his co-workers, 1950-56). Such a pigment (or pigment -mixture) has not been isolated, but Borthwick and his colleagues (1948-54) speculated that it is an open-chain tetrapyrrol pigment, a distant relative of chlorophyll. With its aid a photosynthetic reaction takes place, the nature of which is unknown ^ with the probable result that one or more plant hormones,^ perhaps both activating and inhibiting in their action, travel down the leaf-stalk and up the shoot to influence flowering ; the substance can travel through living cells and across grafts but not across an inanimate obstacle (Cailahian, 1940). The fact that such a substance (or substances) has eluded chemical detection, has stimulated several alternative hypotheses.^ However that may be, and whatever the intimate mechanism, the fact remains that the order of the procession of flowers through the seasons is largely determined by the diurnal periodicity of light and darkness. Bonner. Botan. Gaz., 110, 625 (1949). Darwin. The. Power of Movement in Bonner and Thurlow. Botan. Gaz., 110, Plants, London (1880). 613(1949). Enderle. PZan/a (Berl.), 39, 570, (1951). Borthwick, Hendricks and Parker. Botan. Engel and Heimann. Planta (Berl.), 37, Gaz., 110, 103 (1948). 437 (1949). Borthwick, Hendricks, Toole, E. H., and Engelmann. Pfliigers Arch. ges. Physiol., V. K. Botan. Gaz., 115, 205 (1954). 29, 387 (1882). Borthwick and Parker. Botan Gaz., 100, Fliigel. Planta (Berl.), 37, 337 (1949). 374 (1938) ; 101, 806 (1940). Garner and Allard. J . agric. Res., 18, 553 Borthwick, Parker and Hendricks. Amer. (1920). Naturalist, 84, 117 (1950). Grossenbacher. Amer. J. Botan., 26, 107 Biinning. J6. wrss Bo/an., 75, 439 (1931). (1939). Ber. dfsch. botan. Ges., 54, 590 (1937). Gunn. J. e.rp. Biol., 17, 267 (1940). Biol. Zbl., 64, 161 (1944). Hagan. Plant Physiol., 24, 441 (1949). P/ora, 38, 93 (1944). Hamner and Naylor. Botan. Gaz., \{iQ, Naturwissenschaften, 33, 271 (1946). 853 (1939). A^oYwr/orsc/)., 3b, 457 (1948). Harder and van Senden. Naturwiss- Plania (Berl.), 38, 521 (1950). enschaften, 36, 348 (1949). Ann. Rev. Plant Physiol., 7, 71 (1956). Harder and von Witsch. Gartenhauwiss., Cailahian. C. R. Acad. Sci. U.R.S.S., 12, 15, 226 (1940). 443 (1936) ; 27, 160, 253, 370 (1940) ; Heimann. Planta (Berl.), 38, 157 (1950) ; 31, 949 (1941) ; 47, 220 (1945) ; 54, 40, 377 (1952). 735, 837 (1946) ; 55, 69 (1947). Herms. J. e.r;x Zoo/., 10, 167 (1911). 1 Review, see Lang, 1952. ^ p. 39. 3 See Buiming (1937-50), Bonner and Thurlow (1949), Bonner (1949), Harder and van Senden (1949), van Senden (1951). Recent research indicates that the gibberillins are of fundamental importance in the photoperiodism of plants. LIGHT AND METABOLISM 13 Klebs. i'^ora, 11-12, 128 (1918). Tournois. C. R. Acad. Sci. (Faris), 155, Lang. Ann. Rev. Plant Physiol, 3, 265 297 (1912). (1952). Vegis. Sijmbolae Botan., Upsalienses, 14, Loeb. Pfliigers Arch. ges. Physiol. , 54, 81 1 (1955). (1893) ; 56, 247 (1894). Verworn. Psychophysiologische Protisten- Loehwing. Proc. Soc. exp. Biol. Med., 37, studien, Jena (1889). 631 (1938). Wareing. Ann. Rev. Plant Physiol., 7, Melchers. Biol. Zhl., 56, 567 (1936); 57, 191 (1956). 568 (1937). Wassink,SluysmansandStolwijk.Xonin^-/. Parker, Hendricks and Borthvvick. Botan. tied. Akad. Wetens. Proc, 53, 1466 Gaz., Ill, 242 (1950). (1950). Schubeler. A'«?(/re (Lond.). 21, 31 1 (1880). Wassink and Stolwijk. Ann. Rev. Plant van Senden. Biol. Zbl., 70, 537 (1951). Physiol., 7, 373 (1956). Smith, F. Meld. Norg. LandbrHoisk., 12, Withrow, Withrow and Biebel. Plant 1 (1933). Physiol., 18, 294 (1943). PHOTOPERIODISM IN ANIMALS DIURNAL METABOLIC RHYTHMS are equally remarkable among animals, for the cycle of day and night with its rhythm of changes in illumination, temperature and other environmental factors has so impressed itself upon living creatures in the course of their palaeonto- logical development that many of their metabolic processes vary with a corresponding periodicity, synchronized as it were by an internal physiological clock. These physiological rhythms have received much study and have accumu- lated a considerable literature. ^ Among Mammals, including Man, the periodicity of sleep and activity is the most obvious, ^ possibly a survival of the nocturnal reduction of nervous activity in primaeval Amphibians. Most animals are diurnally active ; but in nocturnal animals the cycle of activity is reversed.^ A similar cyclic variation is seen in bodily temperature. ^^ In Man the temperature through the day is higher than at night, but considerable variations occur in the characteristics of the curve ; in some individuals the peak is in the morning, in others in the afternoon and in others at an intermediate .time. The blood constituents show a variation affecting the haemoglobin, haematocrit readings and plasma proteins,^ while the variation in the eosinophil count is dramatic ; in Man, in the morning there is an eosinopenia* ; in nocturnal animals such as mice the count is high in the morning and low in the early hours of the night.' A similar rhythm acting independently of the intake of fluid affects the urinary output, involving not only the excretion of water but also that of electrolytes (Na, K and chlorides, etc.) and urea which persists even if the 24-hour day is disrupted for periods up to 6 weeks. ^ Even more fundamental cellular processes are involved such as mitotic activity which is maximal in the rest-period at » See Kleitman (1949), Menzel (1952), Halberg (1953). Marker (1958). 2 See Kleitman (1939). 3 Rat— Richter (1922), Browman (1937) ; wood rat— Colton (1933) ; vole— Davis (1932) ; hedgehog— Herter( 1934) ; mice— Achelis and Nothdurft (1939), Aschoff( 1952), Kowalski (1955) ; wikl mice — Johnson (1926). « See Kleitman et al. (1937-38), Kleitman (1949), Halberg et al. (1953). « Renbourn (1947). * von Domarus (1931). ' Halberg and Visscher (1950-52). « Gerritzen (1936-40), Mills (1951), Mills and Stanbury (1952), Mills et al. (1954), Lewis et al. (1956), Lewis and Lobban (1956). 14 THE EYE IN EVOLUTION midnight and minimal at noon, a rhythmic variation first noted in plants ^ and discovered in mammalian tissues (including the corneal epithelium) by van Leijden (1917), confirmed in the human epidermis by Cooper (1939) and noted in the cornea of tadjDoles by Meyer (1954).^ It is interesting that it is a physio- logical process not seen in cancer cells. As will be fully discussed in a subsequent volume, a diurnal variation of soine 3-5 inin. Hg occurs in the ocular tension.^ Established by constant repetition, these rhythms persist for some time in the absence of environmental reinforcement when the external rhythm has been artificially altered or has ceased. The mechanism of these changes is unknown ; most of them are probably maintained by rhythmic changes of activity in the neuro -vegetative centres of the diencephalon, while the endocrine system, particularly the pituitary 70 1^50 =^ 30 ^ ^ eo 'H;^^^;^^:.^^^ 10 0 8 '° ^M» Fig. 8. — The Normal Diurnal Variation in the Intra-ocular Pressure. The abscissae are times of the day ; the vertical line denotes when the patient was asleep. complex, probably has some effect. Apart from the long-known centres controlling thermo-regulation and urinary output, functions such as the variation in circulating eosinophils are governed by the diencephalo-hypophyseal system through the secretion of cortico- steroids by the adrenal cortex (Hume, 1949 ; Porter, 1953), and the evidence is rapidly accumulating that a region in the same neighbour- hood exerts control over the intra-ocular pressure (v. Sallman and Lowenstein, 1955 ; Gloster and Greaves, 1957). However they are controlled, these rhythms are real and autochthonous. Thus in man the normal variation in temperature persists for a considerable period after the commencement of habitual night work, and the diurnal rhythm of urinary flow survives a uniform intake of fluid throughout Kellicott (1904). See Blumenfeld (1939), Halberg (1953). Mailenikow (1904) ; see Duke-Elder (1952). See also p. 560. LIGHT AND METABOLISM 15 the 24 hours and the reversal of the sleep habit. Similarly, the normal phasic swing of the ocular tension is independent of the blood pressure, osmotic changes in the blood, illumination, the time of meals, feasting or fasting, or bodily activity ; the rhythm can only be altered by a complete reversal of the sleep habit established over some time (Raeder, 1925) (Fig. 8). The fact that such rhythms as the diurnal variation in temperature in the new-born infant, or the 24-hour periodicity of activity of the newly hatched chick kept under constant laboratory conditions (Aschoff and Meyer-Lohmann, 1954), are apparent from birth indicates that at any rate some of these fluctuations are fundamental and innate — an environmental influence of biological value which has with time so impressed itself upon organisms that it has become hereditarily transmitted. Some of these diurnal variations, however, seem to depend on environ- mental stimulation. Thus the cyclic variation in the eosinophil count of mice was found by Halberg and his associates (1954) to be abolished by the enucleation of both eyes, although it partially returned some 5 months after blinding. The rhythm of diurnal activity of the minnow, Phoxinus, is said to be reversed on blinding (Jones, 1956). In man the variation in eosinophilia depends to some extent on activity (Halberg et al., 1953), and illumination has a subsidiary influence (Appel and Hansen, 1952 ; Landau and Feldman, 1954). The same rhythms in general activity are seen in Invertebrates, among which Insects provide some of the most dramatic examples (see Welsh, 1938 ; Wigglesworth, 1953). The habit of nocturnal activity and diurnal catalepsy show^l by the stick-insect, Dixippus, for example, persists unchanged for some days in permanent darkness or in reversed illumination (Steiniger, 1933), a daily rhythm which applies to such activities as defsecation and ovij^osition (Kalmus, 1938). The same general tendency is seen in many other species.^ The rhythm may, indeed, be acquired in the larval stage in response to diurnal changes of light, persist through the pupal stage and determine the activity in the adult. 2 A metabolic rhythm in which the CO2 is higher (some- times by 30%) during the night even although the animal is kept in constant darkness is seen in Crustaceans.^ A similar diurnal rhythm of the opening and closing of the valves of the clam, Venus mercenaria, persists under laboratory conditions of constant illumination ; it is interesting that in this case there is also a persistent tidal rhythm and the interaction of the two produces a lunar cycle (Bennett, 1954). A similar phenomenon whereby an endogenous tidal rhythm displaces ^ It is seen in some forest insects (Lutz, 1932 ; Park and Keller, 1932), mayflies (Harker, 1953), cockroaches (Gunn, 1940 ; Mellanby, 1940 ; Marker, 1954), millipedes (Park, 1935), and other species. 2 In Leptinoiarsa — Grison (1943). ^ The crab, Carcinus — Menkes (1952) ; the woodlouse, Oniscus — Cloudesley- Thompson (1952). 16 THE EYE IN EVOLUTION the endogenous diurnal rhythm, is seen in the fiddler-crab, Uca (Brown et al., 1952-54) and also in marine forms of the protozoon, Euglena (Pohl, 1948). A lunar as well as a diurnal rhythm of activity and oxygen consumption is seen in the earthworm, Lumbriciis (Ralph, 1957), and in crayfish such as Cambarus virilis (Guyselman, 1957). The timing of these rhythms with respect to the solar day when the animals are kept in darkness has been altered by lowering the tem- perature (the fiddler-crab, Uca, Stephens, 1957). ^ THE SEXUAL CYCLE OF ANIMALS, as with flowering in plants, is also frequently determined by the influence of light as expressed by the gradual change in the length of day in the annual solar cycle ; in this way the onset of the breeding season becomes rhythmic as though there has been implanted on the central nervous and hormonal systems a pattern of behaviour automatic and innate so that it can only be altered experimentally by a prolonged disturbance of the natural phases. In some species, it is true, particularly in Invertebrates and the lower Vertebrates, other factors such as temperature and humidity also enter into the question, but controlled experiments have shown that these and other extraneous circumstances, such as physical activity and feeding, are often secondary and in many cases can be excluded and that the most important factor is the duration of the period of light — not its intensity or wave-length. These phenomena have been particularly studied in animals inhabiting the northern hemisphere. Spring in these regions with its increasing days is the appropriate season for reproduction if survival is to be maintained, and in those species with a long gestation period, the shortening days of autumn are most suitable for mating. In general, when species with a breeding periodicity of this type are experimentally subjected to artificially lengthening days in late autunrn or winter, they can be brought from their sexually quiescent condition into the ripeness typical of spring, while conversely, if the lengthening days of spring are artificially curtailed, sexual regression occurs ; indeed, it is possible by these means to bring some types (birds, for example) into breeding condition several times in the year — a change which applies not only to anatomical considerations such as the development of the gonads, but also to those habits and modes of conduct which are 'essentially sexual in origin such as (in birds) singing and migration. Such phenomena have been investigated in many species of Inverte- brates, Fishes, Amphibians, Reptiles, Birds and Mammals. In the INVERTEBRATES, even among Protozoa, Ehret (1951) found that the diurnal rhythm of the mating reaction of Paramceciuni bursaris persists for several days in complete darkness and can be altered by varying the illumination ^ Compare p. 22. LIGHT AND METABOLISM 17 at different periods of the daily cycle. In snails, a prolongation of the diurnal period of light beyond 13 hours stimulates egg-laying, while periods of 11 hours or less inhibit it (Jenner, 1951) ; it is interesting that short intervals of illumina- tion during the dark periods of a short-day cycle stimulate egg-laying, showing that, as with short -day plants, the length of the dark period is an essential feature in the stimulus. Similarly the strawberry -root louse. Aphis forbesi, can be made to breed in midsummer instead of February by artificially curtailing the summer days (Marcovitch, 1923). A more dramatic influence is seen in the plant-louse, Psylla : individuals hatched in autumn differ from those hatched in spring but the winter-type can be produced in spring by subjecting the larv£e to an artificial diurnal rhythm in which the period of light is shortened (Bonne- maison and Missonnier, 1955). Among FISHES, temperature has been shown to be a potent factor, but it has been demonstrated that the reproductive cycle of the trout can be photo- periodically determined (Hoover and Hubbard, 1937) ; similarly the activity of the gonads of certain amphibians such as the clawed toad, Xenopus Icevis, (Shapiro and Shapiro, 1934) and reptiles such as the lizard, Anolis carolinensis (Clausen and Poris, 1937), has been altered by means of artificial illumination. BIRDS show more dramatic changes than most species, and these have received much attention probably because of their obvious habits of migration and singing, the sexual connection of which has been recognized since the time of ArLstotle. For long the annual rhythm of the avian gonad was held to be determined bj^ temperature. It is true that in the old custom of " muit " long prevalent in Holland, birds were brought into song in autumn by confining them in the dark in the middle of June and exposing them to light in September, and that by the similar ancient practice of "yogai", Japanese pet birds were brought into singing condition in January by providing them with extra hours of illumination in the autumn (Miyazaki, 1934). In this respect, however, zoologists waited on botanists ; for although Schafer (1907) had suggested that migration, because of its accurate periodicity, must depend on the mathematically regular changes in length of day rather than on the notoriously irregular variations in climate, it was not until the work of C4arner and AUard on the influence of photo- periodism on the flowering of plants had been published in 1920 ^ that Eifrig (1924) propounded a similar hypothesis to explain the habits of birds, a con- ception eventually proved by the experimental work of Rowan (1925-38). Rowan's classical work was on the junco finch, which migrates from wintering grounds in the middle United States to Alberta ; he found that even if the birds were retained in an aviary in Alberta, provided they were subjected to the artificial increase of daily illumination (2-3 mins.) that they would have experienced in the early spring in the States, their gonads matured and they bvirst into song in December despite the temperature of the Canadian winter (minimum, — 50^F). These results were confirmed by Bissonnette (1930-32) in Connecticut experimenting on starlings ; and it is now amply established that among many birds of the temperate zones of the northern hemisphere, the testes of which normally reach a peak of activity as the days lengthen in late . spring, an artificial increase of the period of illumination over some time brings on a precociovis activity, while a curtailment or denial of light brings on the reverse changes.- On the other hand, confinement of male parrots in continuous 1 p. 10. 2 See among others : junco, Junco hyemalis — Rowan (1929), Jenner and Engels (1952) ; starling, Slurnus vulgaris — Bissonnette (1930-32) ; pheasant — Martin (1935), B. C. Clark et al. (1936-37) ; house span-ow. Passer domesticus — Riley (1936), Kirsch- baum and Ringoen (1936) ; white-throated sparrow — Jenner and Engels (1952) ; S.O. — VOL. I. 2 THE EYE IN EVOLUTION darkness for a month results in testicular activity, while continuous illumination produces a resting state (Vaugien, 1952). The same result follows a " natural " change in the day-night cycle, for if the birds in the northern hemisphere are transported to the southern, their breeding season is reversed (Rowan, 1926) ; while in regular migrants across the equator the stimulus for the recrudescence of sexual activity and enlargement of the gonads is the shortening of the days in March in southern lands (Rowan, 1938), an inherent habit which can only be broken if such species are retained for several years in the southern hemisphere and prevented from migrating (Marshall, 1937 ; Baker and Ranson, 1938). It would therefore seem established that the sexual cycle and the migration of birds, rhythins which have become innate, are determined essentially by photo- period, although it is to be remembered that periods of darkness may have an influence equal to or even more potent than light (Hammond, 1953 ; Kirk- patrick and Leopold, 1953), while temperature also has an adjuvant effect (Bissonnette, 1937 ; Farner and Mewaldt, 1952-53 ; Wilson et al., 1956). Similarly among mammals, male ferrets,^ mice ^ and ewes ^ can be brought into oestrus in winter when normally they are in anoestrus by subjecting them to rhythmic periods of increased illumination for 2 months or more, while the gonads of the field-mouse have been shown to diminish by exposing the animals to increased periods of darkness (Baker and Ranson, 1932).* As would be expected, these changes do not apply to non-seasonable animals ^ or those that reach sexual maturity dviring hibernation ® or aestivation.^ Among those animals in which it is operative, however, and particularly among those with migratory habits, the periodic behaviour thus induced sometimes assumes legendary exactitude, a fact commented on since the days of Pliny ; the cuckoo arrives in England on "Cuckoo Day", the early stream of swifts is expected to arrive on the last three days of April and the big arrival on May 24th, while in the late autumn each year the male markhor is said to descend from the high Hindu Kush into the valleys to meet the females on December 14th precisely, and the rut begins (Burton, 1951).* The mechanism of the action of hght in these photoperiodic activities varies, but in general is mediated through hormones the activity of which is largely determined by stimulation through the eyes. This complex matter will be discussed subsequently,^ but at this stage it is convenient to note that in Crustaceans, several hormones are white-crowned sparrow — Farner et al. (1953) ; dove, Zenaidura macroura — Cole (1933) ; Japanese white-eye, Zosterops — Miyazaki (1934) ; duck — Benoit (1934-35), Radnot (1953-55) ; quail— B. C. Clark et al. (1936-37), Hammond (1953) ; fowl— Radnot (1955), Radnot and Orban (1956). 1 Bissonnette (1932), Marshall and Bowden (1934-36), Hart (1951), Thomson (1954). 2 Whitaker (1936). » Hafez (1951). * For further details of the mechanism involved, see p. 559. 5 Guinea-pigs — Dempsey et al. (1933-34) ; rabbit — Smelser et al. (1934). « Squirrel— Wells (1934-35), Johnson and Gann (1933). ' Alexander and Bellerby (1935-38), Bellerby (1938). * In a similar manner the palolo (Polych^te) worms of the South Pacific shed their eggs or sperms in countless millions, sufficient to give the sea the appearance of vermicelli soup, at a specific time. These are eminently edible, and the natives of Samoa have learned to expect a great feast precisely at dawn one week after the November full moon. * p. 547. LIGHT AND METABOLISM 19 secreted in the eye -stalks and central nervous system and stored in the sinus glands and these regulate ovarian maturation and testicular development. In Vertebrates the pituitary gland exerts an analogous gonadotropic influence under the control of its associated centres in the diencephalon which in turn receive their stimulation from the retinae. 1 PHOTOPERiODiSM IN PIGMENT MIGRATION. Pigment, the fuuction of which is so closely related to light, would be expected to be peculiarly susceptible to its influence ; in its migration to cause colour changes,^ rhjrthmic diurnal variations of a primitive type frequently survive. That a persistent rh}i:hm of this kind occurs in the migration of the retinal pigment ^ in the eyes of a noctuid moth, Phisia garmna, was first reported by Kiesel (1894), an observation which has been repeated in several Arthropods with compound eyes and shown to persist even although the animals are kept for a considerable time in conditions of constant illumination and temperature or are reared from the larval stage in the laboratory in constant darkness.* The effect is well seen in the crayfish in the eye of which there is a tapetal reflecting pigment ^ obscured during the day but unprotected at night so that the eye then assumes an orange glow ; even if the animal is kept in conditions of constant darkness and temj^erature, the diurnal rhythm of orange " eye-shine " at night will continue automatically for months (Welsh, 1941). Similar rh}i;hms affecting the retinal and tapetal pigments are seen in many species of Crustaceans (Henkes, 1952), and it would appear that these pigmentary movements are under hormonal control, a subject which will be discussed in a later chapter.^ Closely associated with the movements of the retinal pigment are the corresponding movements of the rods ayid cones of some of the lower Vertebrates. As with the retinal pigment, these movements are usually a direct response to light, but evidence was produced by Welsh and Osborn (1937) that these elements in the eye of the catfish underwent a diui-nal rhythmic change of position even although the fish were kept in constant darkness ; the mechanism of this rhythmic activity is unknown. The integumentary cliromatopliore sy stein frequently shows similar cyclic activities. The responses of this pigmentary system to light are complex and will be studied in a laier section ^ ; it is sufficient to note here that many animals show a rhji;hmic day-night change of colour wherein they pale by night and darken by day, a rhythm which may persist for a considerable time if they are kept in conditions of constant 1 p. 556. 2 p_ go. 3 p_ 170. * In the beetle, Bolitotherus cornutus — Park and Keller (1932) ; and a number of Crustaceans such as fresh-water shrimps, Macrohrachium and others — Welsh (1930) ; crayfish, Cam6a rws—Bennitt (1932), Welsh (1939-41) ; crab, C7ca— Smith (1948); Brown et al. (1951-54), Kleinholz (1937) ; and so on. 6 p. 165. « p. 547. ' p. 82. 20 THE EYE IN EVOLUTION illumination or darkness.^ Gamble and Keeble (1900) first reported such a cyclic diurnal colour change which persisted under constant illumination in the prawn, Hippolyte varians, but although subsequent work has not confirmed this particular observation (Kleinholz and Welsh, 1937), the phenomenon has been demonstrated in a number of species of both Invertebrates and the lower Vertebrates.- In some cases these diurnal changes are largely masked by other factors such as pigmentary changes adopted to mimic the background,^ but the Figs. 9 and 10. — Diurnal Rhythms in the Pigment of the Crab, Uca. The black and white segments at the top of the graphs and in the corre- sponding position immediately below the graphs represent the normal rhythm of daylight and darkness. The second tier of markings below indicate the experimental variations introduced. Ordinates : the degree of pigmentation expressed in Hogben and Slome's scale, 1 representing complete concentration of pigment, i.e., the light phase, and 5 its complete dispersal, i.e., the dark phase (Brown and Webb, 1949). ! ^ '^^^ ^u\^^^ Aj\ , U-t--^ - - -V-- -V '^- l^ri ] V V ' J U U U U U U LLLLL^Ms, Fig. 9. — The normal diurnal rhythm of pigmentation (dark through the day and light at night) is seen to continue uninterruptedly after the animal has been 9 days in darkness. Fig. 10. — At the beginning of the experiment Uca was exposed to continuous illumination (80 foot candles) from A to B. There is a decrease in amplitude and then a gradual inhibition of the rhythm until eventually the chromatophores change irregularly. At B the animals were trans- ferred to continuous darkness, whereupon the chromatophores becaine almost completely con- centrated and thereafter a normal 24-hour rhythm in phase with solar day-night was observed. effect of the underlying rhythm is seen in the increased rapidity of these secondary responses when they are in phase with the primary diurnal cycle and their sluggishness when they antagonize it. In other animals the fundamental rhythm is preponderant so that secondary 1 8 to 9 weeks in the beach-louse, Idotea — Menke, (1911) ; 18 days in the lizard, Anolis — Rahn and Rosendale (1941) ; and so on. ^ Several Invertebrates such as the black sea-urchin, Diadema antillarum — Millott (1950) ; many Crustaceans in addition to Idotea : the prawn, Paloemon — Keeble and Gamble (1904), the fiddler crab, Uca — Abramowitz (1937), the Isopod, Ligia — H. Smith (1938) ; a few Insects such as the stick-insect, Dixippus — Schleip (1910). Compare, for example, Figs. 64-68. A number of Vertebrates, particularly in their youth (Cf. Figs. 70 and 73) ; Cyclo- stomea such as the lampern, Lampetra — Young (1935), Jones (1955) ; Amphibians such as salamander larva* and frogs — Hooker (1914), Welsh (1938) ; and Reptiles such as the American horned "toad", Phrynosortui — Redfield (1918), the lizard, Anolis — Rahn and Ro i»ndale (1941), and the chameleon — Zoond and Eyre (1934). 3 p. 82. LIGHT AND METABOLISM 21 environmental factors have but a slightly modifying effect upon it. A good example of this is the crab, Uca, the responses of which have been extensively studied i ; the diurnal rhythm of its colour change is remarkably constant, and within wide limits is independent of influences such as humidity and temperature, but the influence of metabolism on the phenomenon is exemplified in its retardation with a lengthening of the cycle on exposure to cold below 6° C (Figs. 9 and 10). This rhythmic mechanism operating to disperse pigment in the day phase and concentrate it in the night phase of the cycle would seem to be adaptive in function, partly protective against deleteriously bright illumination, partly thermo-regulatory. In all species in which these colour changes occur the controlling factors are hormones differing in nature from the retinal pigment hormones but, like them, elaborated in Invertebrates by the neuro -secretory system and in Vertebrates by the neurohypophysis both of which show an endo- genous rhythm. This question will be discussed in a subsequent chajDter.^ The seasonal changes in colour of the coats of many Birds and Mammals are analogous phenomena which are also to some extent determined by photoperiod. It is well known that the majority of common birds undergo a post-nuptial moult immediately after the breeding season and a second pre-nuptial moult in spring when they assume their wedding robes. The times at which birds assume their nuptial and winter plumages are governed by a number of factors, the most potent of which is a pituitary hormone with an inherent cyclic activity depending in part on the length of the daily light periods (Witschi, 1935 ; Bro\\Ti and Rollo, 1940 ; Lesher and Kendeigh, 1941 ; Kobayashi and Okubo, 1955). A similar control operates the seasonal moulting of many northern Birds and Mammals the colours of which change from a sinnmer brown to a winter white. Among Birds, the ptarmigan of the northern tundra or the high mountains (Host, 1942), and among Mammals the varying hare (Lyman, 1943) and the ermine (Bissonnette and Bailey, 1944) are good examples of this ; these phenomena of moulting and change of colour can be induced out of season by artificially varying the diurnal periods of ilkimination. It is interesting that in the hare the eyes seem to be the normal receptors of this stimulus since if these are masked the changes do not occur. The pituitary seems to be the only endocrine gland involved since castration and thyroidectomy in the hare are without effect (Lyman, 1943), while hypophysectomy abolishes the cyclic moulting of ferrets (Bissonnette, 1935-38). PHOTOPERiODiciTY IN BiOLUMiNESCENCE. The ability to produce light occurs widely but sporadically among bacteria, fungi, and most types of animals 1 Abramowitz (1937-38), Browii and Webb (1947-49), Brown and Sandeen (1948), Webb (1950). 2 p. 547. 22 THE EYE IN EVOLUTION from the Protozoa to the chordate Fishes ; it is a phenomenon which will be discussed in greater detail later. ^ It is well known that in most animal species the reaction appears intermittently in response to various stimuli, light having a general inhibitory effect, sometimes directly by destruction of the photogenic material in the light-producing cells, sometimes indirectly, acting through a central regulatory mechanism, hormonal or nervous (Harvey, 1925 ; Heymans and Moore, 1925 ; Moore, 1926). In the present connection it is interesting to remark that in a number of species there is a daily rhythm in the capacity to luminesce, a phenomenon seen even in unicellular Dinofiagellates (Harvey, 1952); and in some types of Insects ^ and perhaps in some jellyfish^ and a balanoglossid * the rhythm may persist for several days so that the animal will light up at the normal time of the day even if kept in constant darkness. A final expression of diurnal, khythmicity is seen in the time -memory OF SOME AUTHROPODS AND BIRDS. This curious and interesting phenomenon was first demonstrated in bees by von Stein-Beling (1929-35) who showed that within a cycle of 24 hours bees could be trained to visit an artificial feeding station at regular occasions throughovit the day, a habit which could not be maintained if an attempt were made to operate within a cycle greater or less (e.g., 19 hours) than the normal solar diurnal rhythm. This ability has since been verified by a number of observers ^ and it has been confirmed in wasps ® and ants ^ as well as in the Amphipod Talitrus.^ So far as honey -gathering insects are concerned it is probably connected with the hours at which flowers periodically offer their nectar, but other activities are also involved. Thus Kalmus (1935) found that if larvae and pupse of Drospohila — an insect which normally emerges from its pupa before dawn — were kept in darkness during the daytime and artificially illuminated for 3 consecutive nights, the flies emerged in the evenings, remembering the time of the artificial dawn even although kept in perpetual darkness. Such time-keeping mechanisms or " internal clocks " are of wide occurrence, keeping time automatically with considerable precision, but regularly set and kept in pace by light stimuli. It would seem that the rhythm is influenced metabolically since it can be retarded by low temperatures (under 5° C, Kalmus, 1934) or by drugs ; thus Grabensberger (1934) found that by feeding quinine to trained bees, arrival at the sources of food was retarded, while it was accelerated by iodothyroglobin. A similar apparently innate time-sense can be deinonstrated in some Birds, which we will see ^ assvunes considerable importance in their extraordinary ability to navigate over long distances. Thus Stein (1951) found that passerine birds could be trained to coqie to feed at a particular hour each day provided only that a 24-hour cycle were maintained, an acquirement retained for some considerable time although the birds were kept in constant illumination or had irregular feeding times ; experimental exposure to irregular periods of light and darkness, however, tends to disorientate this sense when it is used as an aid to navigation (Matthews, 1953-55). 1 p. 736. 2 Such as the firefly, Photinus—Bxic'k (1937). ^ Pelagia — Heymans and Moore (1924-25). * Ptychodera—CrozieT (1920). 5 Wahl (1933), Kalmus (1934-54), Kleber (1935), v. Frisch (1937), and others. 6 Verlaine (1929). ' Grabensberger (1934). 8 Pardi and Papi (1952-53), « p. 63. LIGHT AND METABOLISM 23 Abramowitz. Biol. Bull., 72, 344 (1937). J. exp. Zool., 76, 407 (1938). Abramowitz and Abramowitz. Biol. Bull 74, 278 (1938). Acholis and Nothdurft. Pflilgers Arch. ges. Physiol., 241, 651 (1939). Alexander and Bellerby. J. exp. Biol., 12 306 (1935) ; 15, 74 (1938). Appel and Hansen. Dtsch. Arch. klin. Med., 199, 530 (1952). Aschoff. Pflilgers Arch. ges. Physiol., 255, 189, 197 (1952). Aschoff and Meyer-Lohmann. Pfliigers Arch. ges. Physiol., 260, 170 (1954). Baker and Ranson. Proc. roy. Soc. B, 110, 313 ; 112, 39 (1932) ; 113, 486 (1933). Proc. zool. Soc. Lond., 108A, 101 (1938). Bellerby. J. exp. Biol., 15, 82 (1938). Bennett. Biol. Bull., 107, 174 (1954). Bennitt. Physiol. Zool., 5, 65 (1932). Benoit. C. R. Acad.Sci. (Paris), 199, 1671 (1934) ; 201, 359 (1935). C. R. Soc. Biol. (Paris), 118, 664, 669, 672; 120,136,905,1326(1935). Bissonnette. .4wer. J. ^4?k;/., 45, 289 ; 46, 477 (1930). J. exp. Zool., 58, 281 (1931). Physiol. Zool., 4, 542 (1931) ; 5, 92 (1932). Proc. roy. Soc. B., 110, 322 (1932). Anat. Rec, 63, 159 (1935). Wilson Bull., 49, 241 (1937). Endocrinology, 22, 92 (1938). Bissonnette and Bailey. Anti. N.Y. Acad. Sci.,^5, 221 (1944). Blumenfeld. Science, 90, 446 (1939). Bonnemaison and Missonnier. C. R. Acad. Sci. (Paris), 240, 1277 (1955). Browman. J. exp. Zool., 75, 375 (1937). Brown, Fingerman and Hines. Biol. Bull., 106, 308 (1954). Brown, Fingerman, Sandeen and Webb. J. exp. Zool., 123, 29 (1952). Brown and Rollo. T/ie.4!shburn (N.Y., 1936). * See fur p. 107. LIGHT AND MOVEMENT 31 Romanes. Animal Intelligence, X.Y. Verworn. Psychophysiologische Protisten- (1883). studien, Jena (U Russell. The Behaviour of Animals, 2nd. Volta. Galvanismus u. Entdeckung d. Ed., London (1938). Sdulenapparates (1796-1800). Sachs. Vorlesungen iiber Pflanzen physio- Willis. De motu animalium, London Zo^/c, Leipzig (1882). (1670). The Types of Motorial Responses The behavioural responses of organisms to hght are diverse and for three-quarters of a century workers in this field have made numerous attempts to rationalize them into a single system of classification. While terminology itself cannot claim to be an end of science — and, indeed, its apparent definiteness is often misleading — the labelling and classification of phenomena are of great value in the economy and clarification of thinking. Adequate classification, however, entails fundamental knowledge and it is not surprising in a subject which is still highly controversial and inadequately understood that agreement has not yet been reached. In this connection several terms have been introduced into the literature. Strasburger (1878) in his revolutionary work on botany, wherein he made a fundamental study of the movements of plants, used the term phototropism ((f)U)s, (fxjoTos, hght ; TpoTirj, a turning) to describe the mov^ements of sedentary plants in contradistinction to phototaxis (rants', a precise arrangement) to describe the locomotor reactions of freely moving organisms to light. Shortly thereafter, Engelmann (1883) introduced the term kinesis (/ctvi^at?, a movement) to indicate reactions wherein the \-elocity of movement depended on the strength of the stimulus. The next contribution to terminology was due to Pfeffer (1904) who introduced the useful differentiation of phobotaxis (^o'jSo?. fear) to describe random, trial-and-error avoiding naovements, and topotaxis (totto?, a place) to indicate directional attraction movements, while Kiihn (1919-32) subdivided the latter into four categories of increasing complexity in responso, which we shall adopt — tropotaxis, telotaxis, menotaxis, and mnemotaxis.^ To these, Gunn and his colleagues (1937) added the term kxinokinesis and klinotaxis {kX'lv oj, bend) to express changes in orientation determined by turning movements. The term scototaxis {aKoro?, dark) suggested by Alverdes (1930) and Dietrich (1931) is probably unnecessary since those movements which may be interpreted as the result of an attraction to darkness are probably best looked upon as a negative phototaxis. It is true that against this urge for classification some have rebelled (Mast, 1938), but although the dangers of a system of classification in concealing ignorance are obvious, its advantages are so considerable that as a tentative measure we will base oiu" terminology on the classical scheme of Kiihn, introduc- ing some modifications advanced by Fraenkel and Gvmn (1940). It is to be remembered, however, that the tj^^es of response are by no means mutually exclusive and that in their activities many animals show a combination of reactions. A somewhat revolutionary view has recently been advanced by Viaud (1948). He divided the reactions of animals to light into two types : 1 p. 43. 32 THE EYE IN EVOLUTION (a) " Dermatoptic sensitivity'', a "primary" reaction of proto- plasm to light evident throughout the cell in Protozoa and particularly in the surface layer in Metazoa ; and (6) "visual sensitivity", a characteristic of specific photoreceptor organs. The first tyjDe of reaction is concerned with simple attraction towards (or repulsion from) light ; the second is concerned with orienta- tion. The first has two distinct and reciprocal phases : the essential reaction is attraction towards the light (phototropism), purposeful in nature, elicited most readily by short-waved light, the response varying as the logarithm of the intensity of the stimulus (the Weber-Fechner law). Repulsion from light (photoi^hobism), on the other hand, is a negative reaction, a phase of adaptation and recuperation in which the animal flees from light at its own particular speed. Visual sen- sitivity, on the other hand, is confined to the eyes and, concerning itself solely with visual orientation, responds most readily to stimula- tion by the mid-region of the spectrum. The first type of reaction is prepotent in lowly forms (such as Hydra) but becomes masked in higher forms by the second, although it again determines the animal's conduct when it is blinded (Crustaceans such as Dajylmia, Rotifers such as Asplanchna) ; it cannot be elicited in forms higher than Amphibians. The second type of reaction does not appear in the lowest forms and in the higher adds visual apperception to its original function of spatial orientation. This is an interesting although some- what speculative philosophy, and although all the complex story of orientation to light cannot be fitted into it as it stands, it may perhaps contain much truth. In the scheme to be adopted here, the motorial responses of organisms to light will be divided into two main classes : (a) PHOTOKINESES, non-cUrectional changes in random movements. This implies merely a change of activity depending on the intensity of the stimulation, not on its direction ; for its initiation a mechanism is required sensitive only to changes in intensity ; there is no true orientation and the direction of the response is merely a matter of weighted chance. (6) DIRECTIONAL ORIENTATIONS towards (positive) or away from {negative) the stimulating light. The term phototropism will be retained to indicate the directional orientation of parts of sessile plants and animals ; while the translatory movements of motile organisms will be described as phototaxes. It is obvious that these directional responses are more efficient and purposive than the more primitive changes ir-, --ndom activity, since they allow the organism to adapt itself mo: rapidly to the most favourable location in its environmcii . LIGHT AND MOVEMENT 33 To retain a sense of proportion it is well to remember that forms of stimula- tion other than light are operative on living organisms, although none shows the same interest and complexities in the responses elicited. The scientific conception of GEOTROPISM in plants to describe the effects of gravitational influences was introduced by Knight (1806) at a very early date, even before de Candolle (1832) formulated his theory of phototropism. Towards the end of the 19th century however, the study of the responses of organisms to various stimuli rapidly widened. In ec^ually fundamental researches on the action of chemicals on the sperm of ferns and mosses, Pfeffer (1883-88) introduced the term chemotaxis, Stahl (1884) described hydrotropism in fungi, Wortmann (1883) discovered THERMOTROPISM, and Verwom (1889) thigmotropism (contact stimulation ; diyixoL, touch) and galvanotropism. These, however, are not our present concern, and we shall proceed to exemplify shortly the various types of response to light. It is also to be remembered that these various responses may be mutually additive ; thus some flat worms are photo -negative and at the same time swim towards a cathode. When the two stimvili are presented together the response depends upon the direction and strength of each. Thus when the light and the cathode are at right angles the worm will swim at an angle bisecting the direction of the stimvili when the density of the current is proportional to the logarithm of the intensity of the illumination. Alverdes. Z. wiss. Zoo/., 137, 403 (1930). Claus, Grobben and Kiihn's Lhb. der Cailahian. C. R. Acad. ScL, U.R.S.S., 27, Zoologie, Berlin, 246 (1932). 160, 253, 374 (1940). Mast. Biol. Bev., 13, 186 (1938). de Candolle. Phusioloqie vegetale, Paris Pfeffer. Ber. dtsch. botan. Oes., 1, 524 (1832). (1883). Dietrich. Z. mss. ZooZ., 138, 187 (1931). Untersuch. botan. Inst. Tubingen, 1, 362 ^""'iTZn^H^r'' ^"'- '''■ '''"""'' P^a'''l^S^r776 (1904). tfU, yo U»m;. ^, ^ . , ,. , Sfahl. Bo/««. Z., 42, 145, 160, 187 (1884). Fraenkel and Gunn. TAe Onentatwn of gtrasburger. Jena. Z. Naturw., 12, 551 Animals, Oxon. (1940). (1878) Gunn, Kennedy and Pielou. Nature Verworn. ' Psydiophysiologische Protisten- (Lond.), 140, 1064 (1937). studien, Jena (1889). Knight. P/n7os. Tra/is. B, 96, 99 (1806). Viaud, Le photoiropisme animal, Paris Kiihn. Orientierung der Tiere im Raum, (1948). Jena (1919). Went. Rec. Trav. botan. Neerl., 25, 1 Bethes Hb. norm. path. Physiol., 12 (1), (1928). 17 (1929). Wortmann. Botan. Z., 41, 457 (1883). PHOTOKINESIS KINESES [Kivrjois, movement) are the most simple responses of motile organisms to light — they are merely the alteration, either a quickening or a slowmg, of normal random movements witJiout specific directional orientation ; all that is required for their initiation is a mechanism of the simplest type which possesses the ability to react photochemically to variations in the intensity of illumination ; specific photoreceptors (eyes) are in no sense necessary. The phenomenon is essentially the same in character as the alterations in metabolic activity produced by light which we have lately considered. It must be remembered, however, that a motorial response of this type but frequently more dramatic in nature may result from other stimuli such as variations in temperature or moisture. 1.0.— VOL. /. 3 34 THE EYE IN EVOLUTION King-crab Whip-tail scorpion Lamprey Cockroach The response may involve a change of velocity (orthokestesis) {opdos, straight) or a change in direction (kllnoklnesis) {kXlvco, turn). ORTHOKESTESIS, wherein random movements are accelerated or decelerated according to changes in the intensity of the illumination, is seldom the sole mode of response of any organism to light but usually reinforces reactions of another type. In its most dramatic form the organisms move while the stimulus acts, that is, so long as an intensity gradient exists ; when the intensity becomes constant they come to rest. Viewed superficially this elementary response gives a false impression of orientation. Thus if the locomotor activity of an organism is increased by light and diminished in darkness, it aggregates preferentially in the shadowed region even if its movements continue to be random, just as the density of vehicular traffic increases as it is slowed in towns and decreases when speed is regained on the trunk roads ; an organism with this reaction of a high kinesis in the light thus appears to show a negative phototaxis but can be said to be negatively phototactic with as much logic as the average motorist may be assumed to delight in traffic-jams. This response of activity in a light -gradient and rest in the shade giving rise to an apparently photophobic tendency to aggregation in the dark is relatively common ; it is seen typically in the Bacterium photometricum which, as its name implies, becomes active only under the influence of light, in many flat-worms,^ in the maggot larvae of various flies, ^ in certain Arthropods such as the king-crab ^ or the whip-tail scorpion,* in primitive Vertebrates such as the lamprey ^ and in the larvae of certain fish such as the herring, Clupea, and plank- tonic animals as a means of depth-control.^ The converse reaction is less common but is well exemplified by the inactivity of the cockroach in daylight and its activity in darkness.'^ In higher forms these simple kinetic responses are less evident but stimula- tion of the eyes by light frequently has a dramatic effect on general activity. This is especially seen in Insects : thus in the cockroach, Periplaneta, exposure to light considerably reduces the threshold of response to other stimuli (Brecher, 1929), and as the intensity of light is increased the beetle, Popillia, walks more quickly (Moore and Cole, 1921). KLiNOKESTESis is of much wider application and interest ; in it a change of direction is involved, so that turning tnovements, normally ^ Planaria—Pe&T] (1903), Walter (1907) ; Leptoplana—Kovey (1929) ; Plagio- s/omwm— Welsh (1933). « Mast (1911), Herms (1911). = Limulus— Cole (1923). * Mastigoproctus giganteus — Patten (1917). ' :i!,^petra — Young (1935). * Vvoodhead and Woodhead (1955). ' ^iuma orientalis — Szymanski (1914), Wills (1920). LIGHT AND MOVEMENT haphazard, are influenced by the intensity of light so that avoiding reactions occur by trial -and -error with the result that a devious path is taken in a general direction away from the light ; in a favourable environment the animal pursues a straight course, but entering an unfavourable environment it turns away. This may be accomplished by creeping or oscillatory movements as in Alg* such as diatoms and desmids (Pfeffer, 1904), by amoeboid movements as in slime-fungi (Stahl, 1884) or the amoiba (Mast, 1911), or by free-swimming move- ments by cilia as in the swarm spores of Algse and some Ciliates (Oltmanns, 1922). In some Cihates, for example, the direction of movement in a uniform environment changes periodically for no apparent reason so that the animal does not travel long in a straight line ; when exposed to illumination the rate of change of direction is 35 ■cipf ca Fig. 13. — Negative Ki.inokinesis in AmN Menotaxis. The ant was returning to its nest, N, with the sun on its left side. On four consecutive places, 1, 2, 3 and 4, it was shaded from the direct light of the sun and the image from the sun was projected from the animal's right by iii^ans of a mirror. On each occasion the animal preserved its initial orienta- tion n-lative to the sun or its image by turning round (Santschi). LIGHT AND MOVEMENT food, in spite of an immense load between their mandibles and in face of all obstacles, has excited admiration and conjecture for centuries. Nevertheless, although considerable intelligence is suggested, the response is largely automatic. Cornetz (1911) observed that if such an insect were lifted up and set down in another place, it set off in the same direction as before whether or not this led to the nest. That the directing influence was the sun was shown by Santschi (1911) who shaded the ant from the sun and deflected its rays by a mirror so that they reached the insect from the opposite side ; each time this was done the ant immediately changed its path so that it maintained the same direction with regard to the reflected rays as it had previously to 69 5^9'pnn 2^ 39'pnn. Fig. 44. — Menotaxis. The orientation of the ant, Lasius niger. The dark Une indicates the route taken by the ant towards its nest, N. The initial part of its journey was orientated at an angle of about 90^ to the sun. At X, the ant was imprisoned in a box for 2.V hours, from 2.39 p.m. to 5.9 p.m. During this time the sun had traversed an angle of 37-5°. On its release, the ant resumed its path again at right angles to the late afternoon sun, deviating from its former path by an angle of 37° (after Brun). the direct rays (Fig. 43). The same reaction was demonstrated in locusts by Kennedy (1945-51), who found that the direction of the marching desert hoppers could readily be changed and that of flying adults momentarily changed by reflecting sunlight onto them with a mirror. At first this response was assumed to be a typical examjDle of the light-compass reaction, but Wellington (1955) broitght forward evidence that it was more probable that radiant heat associated with the reflected light was the more effective stimulus. A still more elaborate response was demonstrated in the classical experiment of Brun (1914) who confined an ant in a box for some hours in the middle of its homeward journey to its nest ; on releasing the insect it set out on a new track, not now towards its nest but deviating from its original route by an angle corresponding to that through which the sun had moved in the interval so that its rays were still received at the same angle as before (Fig. 44). Again, this was initially 70 THE EYE IN EVOLUTION taken to be an example of the light-compass reaction, but the response could be equally explained by orientation by the j^attern of polarization which also shifts with the sun (Griffin, 1953 ; Wellington, 1955). The homing of the honey-bee when dejirived of other optical clues such as conspicuous landmarks^ is determined by the same mechanism (Wolf, 1927 ; von Frisch, 1931). Behavioural experiments have demonstrated that certain insects are not only able to analyse the polarization of light but can retain its pattern in their memory to take account of the alteration in the position of the sun with the time of day (von Frisch, 1950 ; Vowles, 1950 ; Griffin, 1950 ; Stephens et al., 1952) ; by this type of mnemotaxis it is probable that homing remains accurate for long journeys despite the changing position of the sun. It is not to be thought, however, that the homing of the ant need be an entirely visual process. Bonnet (1779-83) first showed that odour trails may be an effective aid (Carthy, 1950 ; Vowles, 1955), and the ability of this insect to improve its path-finding and avoid detours is exemplified in its extraordinary capacity to learn quite complex mazes (Turner, 1907 ; Schneirla, 1929-33 ; etc.). It is interesting that the " danciyig " of bees, the ballet by which they communicate to other foraging bees the direction, the distance and the richness of a discovery of nectar, is also largely determined by the J I ' I j^ I 1 / ; Fig. 45. — The Dance-figures of Bees. (a) The round dance for short distances performed by German and Austrian bees, (b) The " sickle dance " for short distances performed by Dutch and Swiss bees, (c) The figure-of-eight dance for long distances, with the " wagi.:'. '-run " forming the central component of the figure (von Frisch). 1 p. 78. LIGHT AND MOVEMENT 71 polarization pattern reflected from the sky. The coordinated dance which a returned forager performs on the surface of the comb within the hive was described by Aristotle, ^ and in recent times has been most closely studied by von rrisch,^ the Austrian naturalist (1949-54), using slow-motion cinematography and specially marked bees attracted to rich diets placed at different distances in different directions from the hive. For distances closer than 10 metres the returned bee com- municated its news to the rest of the hive by performing a simple circular dance ; for distances greater than this the direction of the food is indicated by using the vertical direction on the surface of the " 11 .1 f/.. A_ u „ "C-:'A- , , " " v.: A_ /■k " fe^ L /c9^^30°ny.H( . ii - „ 'St ,, •1 . :::a:. ^ K .1 •• - ■■ ;■■ A. A. , a 1 Qrub Z3.6.5Z •A-- /I ■/^ '4 VI / 15 ■. " " ., ^^1 -^ ^- ^O^ny.W. V/ " " / " Dachau 30.6.52 Fig. 46. — 1 he " Displacemp:nt Test " in the Orientation of the Bee. This test indicates the abihty of the honey-bee to allow for a change in the position of the sun. In («), marked bees from a hive, St., were allowed to feed on the afternoon of June 29th, 1952, from a feeding place, F, 180 m. away in the direction 30° north of west. The following morning the hive was transported to another entirely unknown landscape of a completely different type. Tlie vast majority of the bees (15 out of 19), without any help from familiar landmarks, went to one of 4 alternative feeding places 180 m. away from the hive and 30^ north of west, ignoring other symmetrically placed feeding places. On the first afternoon the sun had been in the west ; on the second morning the sun stood '\\\ the east ; so that in order to retain the same orientation the Ijees must have been able to calculate and allow for the solar moveinents (von Frisch). comb (the direction of gravity) to represent the direction of the sun's rays outside the hive, the distance of the soinxe of food by the speed of the dance, and the richness of the find by its vigour. The dance takes the form of a squat figure-of-eight, the straight transverse run of which is marked by the liee actively waggling its body with an enthusiasm depending on the richness of the nectar (Fig. 45) ; the direction of this run bears the same relation to the vertical as does the position of the 1 Hist. An'nunL, 18, 624b. 8. See Haldane, Behaviour, 6, 256 (1954). 2 See Fig. 728. 72 THE EYE IN EVOLUTION source of food to the position of the sun at the time, while the speed of the dance varies inversely as the distance (about 10 revolutions in 15 sees, to indicate a distance of 100 metres, 2-5 revolutions to indicate 3,000 metres). The indications of direction attain an accuracy of 3° in good conditions, of distance of up to 100 metres. Moreover, unlike the ant, bees possess an innate time-keeping mechanism whereby they can make compensation for the movements of the sun or changes in the pattern of polarization in the sky as the day progresses, making the appropriate correction in their direction (Fig. 46). It is interesting that there is no component in the dance for a vertical distance, presumably because svich is rarely required in natural surroundings ; and when von Frisch et al. (1953) fed bees on a feeding-table perched on a radio beacon directly above the hive, new foragers were unable to find it. As performed in the hive the waggle-rvin serves to indicate the direction of the food as related to the sun by reference to the vertical as determined by gravity ; occasionally the dance is performed on the horizontal alighting board in front of the hive and in this case the waggle-run points to the actual direction of the feeding place without reference to the sun. Moreover, in different localities different " dialects " are used. Thus, while von Frisch (1950) found that Avistrian and German bees dance in a circle to indicate food near at hand without giving any indication of its direction, Tschumi (1950) and Baltzer (1952) found that Swiss bees, and Hein (1950) that Dutch bees perform a "sickle dance", dancing in a semi-circle the axis of which denotes the appropriate direction to be followed exactly in the same way as the straight part of the figure-of-eight dance indicates this for far distances (Fig. 45b). This extremely complex and highly ritualized pattern of behaviour is an astonishing performance, particularly when it is recalled that the brain of the bee is about one-tenth of an inch in diameter ; it is apparently inborn and instinctive, but its precise implications have to be learnt through experience by the young workers (Lindauer, 1952). The response is disorientated in shadow, resumes its rhythm as soon as a patch of blue sky becomes visible, and can be artificially changed - by the interposition of a polarizing film between the insects and the sun. Moreover, when trained bees are transported from the northern to the southern hemisphere where the direction of the sun's movement to an observer is anti-clockwise instead of clockwise, their foraging movements tend to be reversed (Kalmus, 1956). A somewhat similar or even more complicated " language " is used by scout bees to indicate the position or direction for a suitable new home or swarm. It is clear, therefore, that the orientation of insects out-of-doors, although determined by automatic responses, is an extremely complex affair influenced by many stimuli acting sometimes singly, sometimes in combination ; and it is equally clear that much work will require to be done before their behaviour is fully elucidated, Aqnafir ■ rfhrojwds also make use of polarized light to orientate themselves \^ ile swimming, in some cases reacting to the polarized LIGHT AND MOVEMENT 73 light of the sky, as do Amphipods when seeking their return to the sea (Pardi and Papi, 1952-53), or making use of the polarization patterns which exist between the air-water interface (Waterman, 1954). Such reactions have been demonstrated in 12 species of Cladocera, water- mites and caddis-fly larvae, which tend to swim so that their direction of movement is at right angles to the plane of polarization (Baylor and Smith, 1953). The crab, Ewpagurus, shows a definite response to a change in the direction of polarization (Kerz, 1950) as also do mosquito larvae. The navigation of the small crustacean, Talitrus saltator, as recorded by Pardi and Papi (1952-53) is a fascinating story. These Amphipods normally live in the intertidal zone. Transferred inland, they move towards the coastline whence they came, taking their direction from the angle of the sun ; as with insects and birds their course can be deflected by changing the direction of the incident light by a mirror. If direct sunlight is not available they can orientate themselves by polarized light from patches of blue sky and can be similarly deflected by the interposition of a polarizing sheet ; under a completely overcast sky they are disorientated. As with bees there is also an innate mechanism which allows them to compensate for movements of the sun throughout the day, but, unlike the reactions of the bee, it would seem that the whole mechanism is established by heredity or acquired in early youth and is set in each individual for ever and cannot be changed. Thus specimens on the west coast of Italy move westwards towards the sea, and even when brought to the seaside of the east coast will automatically attempt to travel westward right across country away from the nearby water. The most extraordinary thing about these creatures is that travelling through the night they appear to be able to navigate with reference to the moon. This is the only instance where this has been established and in view of the complication and rapid change of the lunar path across the sky, it would seem to be an extraordinary feat. ORIENTATION TO A VISUAL PATTERN SO that its reception on the retina remains constant corresponds closely in its mechanism to orientation with respect to a source of light. Thus insects placed on a turn-table facing a window will move round when the table rotates (Radl. 1902) and if a striped drum is rotated in front of them they will endeavour to keejD in line with a given stripe (an " optomotor response'") (Schlieper, 1927 ; Schulz. 1931 ; Zeiser. 1934)i. Gregariousness in locusts depends on the same reaction ; moving so that it nullifies the movement of images across its retina, each swarming insect travels precisely with its neighbour (" gregarian inertia "), the whole host being guided by a light-compass reaction to the incidence of the sun's rays (Kennedy, 1939-45). Orientation when swimming against a current of water (" rheotaxis ") is in fact a visual response of the same type : the water-boatman, Notonecta, for example, turns upstream and swims with sufficient strength to maintain a constant impression of the nearby bank ; if the landmarks on the bank are moved, the water- 1 This reaction has been used to measure the visual acuity of insects, see p. 588. Eupagurus Talitrus saltator Locust Xotonecta 74 THE EYE IN EVOLUTION Gyrinid beetle Daphnia boatman moves with them, and if they are obliterated as when swim- ming in the dark or between plain white boards, the insect allows itself to be carried j^assively downstream (Schulz, 1931). Gyrinid beetles are similarly disorientated when swimming in the dark or if a sndden change is made in the landmarks on the banks (Brown and Hatch, 1929). THE DORSAL (ventral) LIGHT REACTION. The Orientation of animals which progress on the earth's surface can be treated as if movement on one plane only need be considered ; but those that swim or fly have three available planes of movement — they can turn as do land animals on a vertical axis, but they can also roll on a longitudinal axis or they can pitch, turning somersaults about a transverse axis (Fig. 48). They must therefore possess a complex means of orientation to maintain the body in a desired position as it travels towards a goal. Because of its relatively greater specific gravity the stability of an animal body in air is greater than in water, and since the attachments of wings are comparatively high making the centre of gravity relatively low, the equilibrium of balance in birds raises no serious difficulties. This does not apply with the same force to insects although some, such as the dragon-fly, Anax, demonstrate a dorsal light response during flight, the effective organ being mainly the compound eye (Mittelstaedt, 1950) ; but aquatic animals require to perform constant and active balancing movements to maintain their normal orientation. Many fishes maintain their position optically by keeping one surface (usually the dorsal) perpendicular to the light, using their eyes as receptor organs ; others have evolved a specific statocyst organ to maintain equilibrium, but although this development has assumed the greater importance eventually, the eyes still participate in the orientating reflexes, a collaboration between the senses which survives in the elaborate reflex connections which continue to yoke the visual with the vestibular system in Man. The dorsal light reaction was initially recognized in the crustacean, Da])hnia, by Radl (1901), and its wide distribution was first appreciated by von Buddenbrock (1914-37) ; it has since been observed in many groups of aquatic animals of a wide variety.^ In its essentials the DORSAL LIGHT REACTION eusures that when the light is above, the animal swims with the dorsal surface upwards, maintaining itself symmetrically to it and moving (if it does move) in a plane at right 1 In Medusaj — Fraenkel (1931) ; polychaete worms — Fraenkel (1931), v. Budden- brock (1937) ; in a large number of Crustaceans — v. Buddenbrock (1914), Alverdes (1926-30). Schulz (1928), Seifert (1930-32) ; among Insects in nymphs and larvje— V. Buddf Ml)rock (1915), Wojtusiak (1929) ; in the dragon-fly, Anax, during flight — ■ Mittelsta. t (1949) ; perhaps in the desert locust, Schistocerca gregaria — Rainey and Ashall (1! '.) ; and particularly in Fishes — v. Hoist (1935). LIGHT AND MOVEMENT angles to it ; if the light is placed horizontally the animal rotates correspondingly, and if the light is placed below, it either rolls or somersaults over to swim belly-upwards (Fig. 47). In the ventral LIGHT REACTION an animal which normally swims belly-upwards behaves analogously (Fig. 48). Occasionally, however, if the normal direction of the incidence of the light is changed, the animal does not Fig. 47. — The Dorsal Lkjht Reaction. On the left half of the aquarium the Crustacean, Apiis, is illuminated from its right side; on the right half of the aquarium, from its left side. As it swims between the two, it orientates itself by rolling on its longitudinal axis (after Seifert). ® ^"■"^^.^^^J Fig. 48. — The Ventral Li(;ht Keaction. The change of orientation in the Crustacean, Artemia salitia, when the light is changed from abo\p to below. Fig. 48«, by a rolling movement ; Fig. 4S6, by a back somersault or pitching movement (in a photo-positive individual) (after Seifert). act reflexly but becomes completely disorientated and swims aimlessly, a reaction seen, for example, in the nemertine worm, Linens ruber, which in normal circumstances is negatively phototactic (GoutcharofF, 1952). The visual mechanism involved varies in different species. In some larvae the response is mediated by the dermal light sense and persists after total blinding (Schone, 1951) but as a rule the eyes are Linens ruber 76 THE EYE IN EVOLUTION A pus implicated. The water-flea, Daphnia, orientates itself in the typical manner by means of a single dorsal median eye ; while the fresh-water crustacean, Apus, has two compound eyes and a median eye on the dorsal surface. Other crustaceans have two eyes ; when one is removed or painted over, rolling and circling movements occur towards the seeing side, and if both are thrown out of action the light reaction disappears (the brine-shrimp, Artemia, Seifert, 1930-32). The relation between the statocyst and the eyes in those animals which possess the dual mechanism was prettily shown by von Hoist (a) (h) \ \ \ t t t Fig. 49. — The Dor.sal Light Reaction. In the fish, Crenilahrus rostratus. Upper two fish. The Hght comes from above ; (a) in the intact animal, (b) in the labyrinthectomized animal. Orientation is normal. Lower two fish. The light comes from below ; (a) the norinal posture is retained owing to the influence of the labyrinth ; (b) the labyrinthec- tomized animal swims in an upside-down posture (after von Hoist). (1935) in the fish, Crenilahrus rostratus. Normally the balance is maintained essentially by the static reactions of the labyrinth which are supplemented by the light reaction. If, however, a light is placed horizontally, a compromise orientation is assumed with the body slightly tilted towards the light, the inclination varying directly with the strength of the illumination ; when the light is placed underneath, the static reactions control the animal and the light is without effect (Fig. 49). When, however, the labyrinths are put out of action, the optical reaction functions in the pure form, the movements of the trunk, the fins and the tail, hitherto controlled by the labyrinth, now being entirely coordinated by the eyes so that with a transverse light the fish swims on its side ; with a light below, upside-down ; finally, when one eye is put out of action, the fish rolls towards the seeing side for a time until an adaptive reaction asserts itself. This reaction, of course, is often combined with other types of phototaxLs. Thus the water-flea, Daphnia, is usually positively tropotactic and also exhibits a compa'is reaction (von Frisch and Kupelwieser, 1913 ; Eckert, 1938), the brine-shrimp, Artemia, may be positively or negatively phototactic, and so on. LIGHT AND MOVEMENT 77 Alverdes. Z. vergl. Physiol., 4, 699 (1926). Z. iciss. ZooL, 132, 135 (1928) ; 137 403 (1930). Antrum and Stiimpf. Z. Naturforccli., 5b, 116 (1950). Baltzer. Arch. Julius Klaus-Stift. Verer- bungsforsch., 27, 197 (1952). Bartels. Z. vergl. Physiol., 10, 527 (1929). Bartels and Baltzer. Rev. Suisse ZooL, 35, 247 (1928). Baylor and Smith. Ainer. Nat., 87, 97 (1953). Bonnet. Observations sur des pet its fourmis. Oeuvres Hist. nat. Philos., Neuchatel. 1 (1779-83). Brown and Hatch. J. cotirp. Psychol., 9, 159 (1929). Brun. Die liauniorientierang d. Anuneisen, Jena (1914). von Buddenbrock. Zool. Jb., Abt. allg. Zool. Physiol., 34, 479 (1914) ; 37, 313 (1919). S. B. Heidelberg. Akad. wiss. Math.-Xat. KL. 6B, 1 (1915) ; 8B, 1 (1917). Z. vergl. Physiol., 15, 597 (1931). Grundriss der vergl. Phi/sinl., Berlin, 1 (1937). von Buddenbrock and Scliulz. Zool. Jb., Abt. allg. Zool. Physiol., 52, 513 (1933). Carthy. Nature (Lond.), 166, 154 (1950). Behaviour, 3, 275 (1951). Cornetz. Rev. Suisse Zool., 19, 153 (1911). Crozier and Wolf. J. gen. Physiol., 27, 287, 315 (1943). Davis. J. appl. Pht/sioL, 19, 307 (1948). Eckert. Z. vergl. Physiol., 25, 655 (1938). Fraenkel. Z. vergl. Physiol., 6, 385 (1927). Biol. Rev., 6, 36 (1931). von Friseh. Aus deni Leben der Bienen, Berlin, 2nd ed. (1931). Experientia, 5, 142 (1949) ; 6, 210 (1950). Bees, their ]'ision. Chemical Senses and Language, Ithaca (1950). Naturwissenschaften, 38, 105 (1951). von Friscli, Heran and Lindauer. Z. vergl. Physiol., 35, 219 (1953). von Friseh and Kvipelwieser. Biol. Zbl., 33, 517 (1913). von Friseh and Lindauer. Naturwissen- schaften, M, 245 (1954). Gordon. Science, 108, 710 (1948). (Joutcharoff. C. R. Acad. Sci. (Paris), 235, 1690 (1952). Griffin. Biol. Bull., 99, 326 (1950). Biol. Rev., 27, 359 (1952). Amer. Sci., 41, 209 (1953). Hein. Experientia, 6, 142 (1950). von Hoist. Biol. Rcc. 10, 234 (1935). Pubbl. Staz. zool. Xapoli, 15, 143 (1935). Honjo. Zool. Jb., Abt. allg. Zool. Physiol., 57, 375 (1937). Ising. Ark-, mat. uslr. Fys., 32, 1 (1945). Kalmus. Nature (Lond.), 173, 657 (1954). J. exp. Biol., 33, 554 (1956). Kennedy. Trans, roi/. entcm. Sac, Lone/., 89, 385(1939) ; 95,247 (1945). Philos. Trans. B, 235, 163 (1951). Kerz. Experientia, 6, 427 (1950). Kramer. The Ibis, 94, 265 (1952). J. Ornith., Leipzig, 94, 194, 201 (1953). Kramer and St. Paul. Z. Tierpsychol., 7, 620 (1951). Verh. dtsch. zool. Ges., 1951 (1952). Lack. Brit. Birds, 37, 122, 143 (1943). Lindauer. Z. vergl. Physiol., 34, 299 (1952). Ludwig. Z. wiss. Zool., 144, 469 (1933) ; 146, 193 (1934). Mattliews. J. Inst. Navigation, 4, 260 (1951). J. exp. Biol.. 28, 508 (1951) ; 30, 243, 268, 370 (1953) ; 32, 39 (1955). r/(e/6i:s, 94, 243(1952) ; 96,432(1954). Behaviour, 4, 202 (1952). Trans. ophthcd.Soc. U.K.. 74, 67 (1954). Bird Navigation, Camb. (1955). Menner. Zool. Jb., Abt. allg. Zool. Physiol., 58, 481 (1938). Menzer and Stockhammer. Naturwissen- schaften, 38, 190 (1951). Mittelstaedt. Naturwissenschaften, 36, 90 (1949). Z. vergl. Physiol., 32, 422 (1950). Montgomery and Heinemann. Science, 116, 454 (1952). Pardi and Papi. Naturwisse)ischaften, 39, 262 (1952). Z. vergl. Physiol., 35, 459, 490 (1953). Pratt and Thouless. J. exp. Biol.. 32, 140 (1955). Radl. Biol. Zbl., 21, 75 (1901) ; 22, 728 (1902). Rainey and Ashall. Brit. J. anim. Behav., 1, 136 (1953). van Riper and Kalmbach. Science, 115, 577 (1952). Ruppell and Schein. Vogelzug, 12, 49 (1941). St. Paul. Behaviour, 6, 1 (1953). Sant.schi. Rev. Suisse Zool., 19, 117 (1911). Schiieper. Z. vergl. Physiol., 6, 453, (1927). Schneirla. C'omp. Psychol. Monogr., 6, No. 30 (1929). J. comp. Psychol., 15, 243, 367 (1933). Z. vergl. Physiol., 19, 439 (1933). Schone, Z. vergl. Physiol., 33, 63 (1951). Schulz. Z. vergl. Physiol., 7, 488 (1928) ; 14, 392 (1931). Seifert. Z. vergl. Physiol., 11, 386 (1930) ; 16, 111 (1932). Stephens, Fingerman and Brown. Anat. Rec, 113, 559 (1952). Ann. entom. Soc. Amer., 46, 757 (1953). Sullivan and Wellington. Canad. Entom., 85, 297 (1953). Tsclmmi. Scliweiz. Bienoi-Zeitung, 129 (1950). 78 THE EYE IN EVOLUTION Turner. J. comp. Neurol. Psychol. ,11, Ml Wellington. Nature (Lond.), 172, 1177 (1907). (1953). Biol. Bull., 13, 333 (1907). Ann. entom. Soc. Amer., 48, 67 (1955). Varian. J. apjd. Physiol., 19, 306 (1948). Wellington, Sullivan and Green. Canad. Viaud and Marx. C. R. Soc. Biol. (Paris), j. ZooL, 29, 339 (1951). 142,249,251,254(1948). Wellington, Sullivan and Henson. Canad. Volkonsky. Arch. Inst. Pasteur Alger., Entom. 86 529(1954). ^T }^' ^\i [^^^^\- Wilkinson. ' Proc. Linn. Soc. Lond., 160, Vowles. Nature (Lond.), 165, 282 (19o0). q. MQ^Q^ J. ea;«. BioZ., 31, 341, 356 (1954). ... •/ , d „ •, , ^ ^ Brit. J. anim. Behav., 3, 1 (1955). ^^ °JVI''%''-o f,"^^ o^ -ui^^L ^ "''''"' de Vries, Spoor and Jielof. Physica, 19, ,,, J^"^^' ^''{-^'Jr^^^^^JT^l'.n.n. 419(1953). ^^°lf- -Z. I'er^^- -P/'y«'o^-, 6, 221 (1927). Waterman, ^c/ence, 111, 252 (1950) ; 120, Yeagley. J. a^pyjL P/;ys;oZ., 22, 746 (1951). 927 (1954). Zeiser. Zool. Jb., Abt. allg. Zool. Physiol., Trans. N.Y. Acad. Sci., 14, 11 (1951). 53, 501 (1934). MNEMOTAXIS MNEMOTAXis is the most complicated method of orientation and allows the animal to deal ivith all the elements of a coynplex situation in the light of experience gained in the past (Kiihn, 1919-39). In the previous reactions we have studied, the response is made to one stimuhis only or the synthesis of several, and it may be either direct as in tropotaxis or indirect as in menotaxis, a simple mechanism which becomes effective by the inhibition of all stimuli but the dominant one. These more primitive taxes determine the reactions of lower species, and although they enter into the total response of the higher animals and can be studied separately in experimental conditions, the normal activities of the latter are rarely based on so simple a pattern of behaviour. It is true that the homing honey-bee can orientate itself with regard to the sun and that this is the only mechanism available to the soaring bird as it rises in strange surroundings, but both also make use of other clues in ordinary life as soon as they can appreciate objects in a known environment. In this more elaborate type of orientation two new capacities are added to one or other of the simpler methods — (1) the ability to integrate a number of stimuli simultaneously instead of inhibiting all but one, and (2) the modification of a direct automatic response by the factor of memory through a process of conditioning. By a synthesis of these factors the animal is thus able to deal with a complex situation as a whole (Adlerz, 1903-9 ; v. Buttel-Reepen, 1907 ; Turner, 1908 ; Rabaud, 1924-26 ; Wolf, 1926-27 ; Hertz, 1929-31 ; Friedlander, 1931 ; Tinbergen, 1932-51 ; Tinbergen and Kruyt, 1938 ; Baerends, 1941 ; and others). In its simplest form this is illustrated by the experimients of van Beusekom (1948) with the homing digger wasp, Philanthus (Fig. 50). The initial training situation to which the wasp was conditioned was a square block set at right angles close to the nest and a model of a tree 1 metre from the nest. In the test experiment the block was turned through 45" and the tree displaced first to one side and tlien the other ; the wasp approached the corner opposite to that LIGHT AND MOVEMENT 79 in which the tree was located as if up to the last moment she used both the tree and the block as landmarks. The prettj^ experiment of Tinbergen and Kruyt (1938) shows the astonishing rapidity and precision with which the wasp learns to relate its nest to neighbouring landmarks and to appreciate a situation as a whole. A ring of 20 pine-cones was placed around the nest while she was inside ; on leaving she made a study of the locality for 6 seconds only (Fig. 51) ; the pine-cones were then arranged similarly one foot away from the nest ; returning after 90 minutes with a captured bee, she alighted in the middle of the ring of cones, a choice repeated T 6 --a- Fig. 50. — The Path of the Digger Wasp, PHiLAyrHcs TRiAyocLcn. On the left, the training situation. The path of tlie wasp ^starting from the circle) is directly to its nest at the angle of the block past the tree. On the right, the test situation. The block is rotated througli 4.5^ and tlie tree moved tirst to A and then to B. The wasp alights alternately at a and b (simplified from van Beusekom). 13 times, and only found the nest after the original situation had been restored (Fig. 52). A still more extraordinary ability is seen in the wasp, Ammophila, which hunts caterpillars too heavy to be brought back on the wing ; as it laboriously drags its prey to the nest it is apparently able, apart from occasional exploratory flights, to utilize the memories of aerial observation, probably aided by light-compass orientation (Thorpe, 1943-56). Behaviour of this type is obviously determined by the iitiHzation of a number of stimuH and experiment has sho^\^l that in making its decision the insect does not condition itself to every available landmark but exercises some degree of choice on principles which would differ from that of a human being. Moreover, the stimuli need not be simultaneous for visual memories may be retained for some considerable time ; thus the bumble-bee, Bombus, will fly regularly round a number of fixed landmarks in the same sequence for weeks on end (Frank, 19-11). Such studies are of unusual interest but our knowledge of the problems they raise is yet very imperfect ; indeed, experiment has just Bombus 80 THE EYE IN EVOLUTION Figs. 51 and 52. — The Reactions of the Digger Wasp. Fig. 51. — The wasp, Philanthus triangulum, on leaving the nest in the centre of the ring of pine cones, makes a locaUty-study lasting 6 seconds and then leaves. Nest ' ■^^ ^ k. Fig. 52. — The ring of pine cones is then displaced from the nest and on her return the wasp alights in the centre of the ring and will only find the nest after the original situation has been restored (Tinbergen, Study of Instinct; Clarendon Press). begun to elucidate the more complex aspects of animal psychology in which the basic instinctive reactions are modified by experience of the past. Adlerz. K.Sveriska Vetensk. Akad. Handl., 37, No. 5, 1 (1903) ; 42, No. 1, 1 (1906). Entom. TidsJ-r.,ZO, 163 (1909). Baerends. T. Entom. (Amst.), 84, 68 (1941). van Beusekom. Behaviour, 1, 195 (1948). von Buttel-Reepen. Naturwiss. Wschr., 22, 465 (1907). Frank. Z. vergl. Physiol., 28, 467 (1941). Friedlander. Z. vergl. Physiol., 15, 193 (1931). Hertz. Z. vergl. Physiol., 8, 693 (1929) ; 11, 107 (1930) ; 14, 629 (1931). LIGHT AND MOVEMENT 81 Kiihn. Die Orientierung der Tiere in Tinbergen. Z. vergl. Physiol., 16, 305 i?aum, Jena (1919). (1932). Grundriss d. allg. Zool., Leipzig (1939). The Study of Instinct, Oxon (1951). Rabaud. Feuill. Nat., 1, 1 (I92i). Tinbergen and Kruvt. Z. vergl. Physiol., Bull. Biol. Fr. Belg., 60, 319 (1926). 25, 292 (1938). Thorpe. Brit. J. Psychol., ii, 220 ; 34, Turner. Biol. Bull., 15, 2-il {1908). 20, 66 (1943-44). Wolf. Z. vergl. Physiol., 3, 615 (1926) ; Learning and Instinct in Animals, 6, 221 (1927). London (1956). J. soc. Psychol., 1, 300 (1930). so.— VOL. I CHAPTER IV THE EFFECT OF LIGHT ON PIGMENTATION The dramatic effects of light on the pigments of plants and animals have long been recognized. The yellowish-white pallor assumed by plants containing chlorophyll confined in darkness is well known, while the diatoms of the Lakes of Anvergne, equipped with green chlorophyll and brown diatomin, change colour according to the depth of the water in which they find themselves (Heribaud, 1894) ; but the most dramatic effects are evident in the integumentary pigments of 2^oikilochromic ^ animals. The spectacular and rapid changes in colour between black and green seen in the chameleon were noted in the fourth century B.C. by Aristotle, while Pliny described somewhat similar changes in the dying mullet. Since classical times a considerable amount of observation and research has been devoted to the subject and a surprisingly wide range of colour changes has been recorded in a large variety of animals — a euglenoid Protozoon, polycheete worms, leeches, Echinoderms, Cephalopods, Crustaceans, Insects, and among Vertebrates, numerous Fishes, Amphibians and Reptiles. 2 Biologically these changes may be assumed to serve two purposes, one the antithesis of the other — cryptic or protective and 'phayieric or demonstrative. The protective function is the more fundamental and the more common, the demonstrative is a later and more rare acquisition.^ The PROTECTIVE FUNCTION is designed in general to allow the animal to adapt itself to its environment and shows three main modifications. In its most primitive form such a variation in jsigment probably developed as a light -absorptive function to provide protection against deleterious light and heat ; occasionally pigmentary variations are apparently thermo-regulatory — an early attempt at thermostasis — as is seen strikingly in some desert lizards in which colour changes may be induced experimentally by changes in temperature alone (Parker, 1906-38 ; Bauer, 1914 ; Kriiger and Kern, 1924 ; -and others). The most common and dramatic colour variations, however, have evolved as an adaptive phenome7ion allowing the animal to become as 1 TToiKi'Aof, varied ; xpuiyi'^, colour. 2 For extensive reviews see van Rynberk (1906), Fuehs (1914), Hogben (1924), Parker (1930-5r.) and Brown (1950). ^ These are r xamples of a large group of phenomena termed allcesihetic by Huxley (1938) which exer! their biological effect through the agency of the distance receptors of another individual — sight, hearing or smell. 82 LIGHT AND PIGMENTATION 83 inconspicuous as possible and obliterate itself in its environment ; and, as we shall see, this faculty of mimicey or homochromatism is sometimes carried to almost unbelievable lengths, particularly among teleostean fishes, the animal not only changing its general appearance in light and shade but assuming the pattern of colour — blue, red, yellow, green, black — of its surroundings (Fig. 53). Fig -The Eukopkan Plaice LEV ROy EVTES PLA 2'Et^--\^:-.i<-^^^^tmuj^ ■' — B Fig. 60. — The epidermis in the light- adapted stage. Fig. 61. — The epidermis in the dark- adapted stage. Salmo triitta comprised of various fat-soluble carotenoids ^ contained in lipophores. In Invertebrates (Crustaceans, Insects) the chromatophores are frequently polychromatic since each may contain a variety of these pigments — blue-green, orange, yellow and red — sometimes each with a separate distribution within the cells.- In Vertebrates the chromato- phores are usually monochromatic — red (within erythroxthores), yellow (within xantho2)hores) or green ^ — one animal often having several types of pigment in different integumentary cells (purple astacene and yellow lutein in the brown trout, Salmo trntta, Steven, 1948). A third pigmen- tary factor is found extensively both in Invertebrates and Vertebrates Figs. 62 and 63. — Colour Changes in the Lizard. Fig. 62. — The deposition of the melano- phores in the brown state when the branches of these cells extend into the stratum germinativum. Fig. 63. — The lizard in the green con- dition when the pigment is con- centrated beneath the static pig- ment in the superficial layers. The stratum corneum has been displaced from the section (Kleinholz). 1 The carotenoid pigments are of wide distribution and great biological interest, playing a part as sensitizers to the phototropic movements of plants, the phototactic movements of animals, and also participating in visual processes. Their nature will be discussed at a later stage (p. 118). 2 In Crustaceans — Kiihn and Lederer (1933), Fabre and Lederer (1934) ; in Insects — Schleip (1910-15), Giersberg (1928). 3 See Fox (1947). LIGHT AND PIGMENTATION 89 — guanine. This may form a white highly reflecting layer, as in Crustaceans, or, as in many Vertebrates, may be contained in white gtianophores or variegated iridocytes, the iridescent colour changes of which are due to the arrangement, form and movements of plate-like crystals of guanine — a form of coloration akin to that due to the diffrac- tion of light by the scales offish and reptiles or the feathers of birds. The colour changes in these cells are sometimes quite remarkable ; thus in the killifish, Fundulus, a single iridocyte may exhibit blue-green, orange, yellow and red phases in successive moments. The factors causing colour changes in animals include extremes of temperature, humidity, contact stimulation, and psychic stimuli, particularly excitement and fear ; but the most general and much the most important is light. Light acts upon chromatophores in one of three ways — by a direct, primary effect on the cells themselves, by a secondary reaction through the eye, or by indirect reactions through receptor mechanisms other than the eyes (the central nervous system and the pineal body). A further response — the endogenous diurnal variation in coloration, largely controlled by hormones and nervous centres situated in the mid-brain — we have already discussed.^ {a) When light acts directly upon the chromatophores themselves the reaction may be called a peimary response. This is the most primitive mechanism and the only one available to unicellular plants (diatoms) or animals {Euglena), but it is frec|uently retained in higher forms, usually as a generalized darkening in the shade and lightening with illumination, a change, however, normally obscured by the more dominant secondary responses through the eyes. The primary response, however, can be observed in young specimens the chromato- phores of which have not yet come under the control of the secondary mechanism, in blinded animals (Osborn, 1940), in denervated regions after nerve section and degeneration, and in isolated fragments of the skin when exposed to illumination, a reaction demonstrated in crustaceans (Keeble and Gamble, 1905) and in some sea-urchins (Kleinholz, 1938 ; Millott, 1954-57) (Figs. 64 to 67). The direct motor resjionse of individual ectodennal cells to the stimulus of light survives among the higher animals in the movements of the retinal rods and cones - and in the contraction of the pupillary mviscles, both of which are ectodermal in origin. In the iris of Cephalopods, Fishes and Amphibia a direct contraction to light commonly occurs,^ and although the primitive response in the higher ^Mammals and man has been replaced by a reflex nevu'o-mechanism, 1 p. 19. " p. "31. 3 Brown-Sequard (1847-.59), Budge (1855), Miiller (1860), Schur (1868), Steinach (1890-92), Magnus (1899), Guth (1901), Marenghi (1902), Hertel (1907), Young (1933), Weale (1956), and others. Fundulus Diatom 90 THE EYE IN EVOLUTION Figs. 64 to 67. — Pigmentary Changes with Light Intensity IN A Sea-urchin. Fig. 65. X ■ i "mk X / Fig. 66. Fig. 67. To show the variation of pigmentation in a young specimen of Diadema antiUarum. In the hght-adapted phase the animal appears uniformly black owing to the dispersion of melanin pigment (Fig. 64). In the dark-adapted phase the melanin recedes from the aboral surface leaving beautifully defined patterns of white lines and a ring, an effect due to the concentration of pigment (Fig. 65). In older specimens, the changes are less marked (Figs. 66 and 67) (N. Millott). LIGHT AND PIGMENTATION 91 it may still be elicited with the more effective stimulus of ultra-violet light after all connections with the central nervous system have been severed. (6) The most dramatic reactions follow stimulation of the eyes (SECONDARY RESPONSES). Hogben and Slome (1931), for example, found that in the case of the clawed toad, Xenopus. when the field of vision was occupied by a light-scattering surface the animal became pale, when set in the dark background of a light-absorbing surface the animal suffered generalized darkening of the skin, a response abolished on removal of the eyes. While the primary responses react in general to the total intensity of light, the secondary resjDonse is usually based on the ratio of the amount of incident light entering the eye directly from above to the amount of reflected light from the back- ground, so that on a dark background, when the ratio is large, the animal becomes dark and on a light background, when the ratio is small, it becomes pale ; it is to be noted that these changes occur without regard to the intensity of the total illumination (Sumner, 1911-40 ; Sumner and Keys, 1929 ; Brown, 1936 ; Sumner and Doudoroff. 1937). This influence of the reflectance or albedo of the background (to borrow an astronomical term) has been fully established by experiment ; thus the effect of a dark background can be faithfully reproduced by makmg the lower half of the cornea opaque ^ ; reversal of the fish or of the illumination or the background produces the expected effect ; and Butcher (1938), on rotating the eye of the killifish, Fu7idulus. through 180°, found that it gave its tawny response to a yellow backgroimd only when the latter was above the animal. In his work on teleostean fishes Sumner (1940) established that the reflect- ance of the substrate had an important effect on morphological colour changes also, for he found that the melanophore count and the total quantity of melanin varied inversely as the logarithm of the reflected light. The mathematical nature of the relationship is interesting and unexpected ; it recalls Fechner's modifica- tion of Weber's Law defining the relationship between the intensity of stimuli and their sensory apjDreciation, and suggests that in assuming control of these colour changes the eye applies the same quantitative standards as govern its sensory activities. In addition to this general quantitative reaction, a differentiated response to the siDectral nature of the light reflected from the back- ground is relatively common so that the animal can assume the colour of its environment, sometimes with remarkable rapidity and accuracy. This apparently extraordinary reaction was first scientifically described in the chameleon prawn, Hippolyte, by Keeble and Gamble (1899) and many instances have now received study. The prawn, Paloemon, for exaniiDle, can manipulate its red, yellow and blue pigments, so that with- 1 In the insert. Di.rippus — Atzler (1930) ; Priebatsch (1933) ; in shrimps — Hanstrom (1937-38) ; in fishes — Sumner (1940). Hippolyte 92 THE EYE IN EVOLUTION Epinephelus Triturus cristatus Phoxinus in a few days it can adapt itself to its habitat by becoming red, yellow blue, green, white or black (Brown, 1935), a facility possessed in some degree by several crabs ^ and Cephalopods.^ Such a change may occur rapidly ; thus the larvse of butterflies (Brecher, 1922) and salamanders (Kammerer, 1920) when placed under variously coloured glasses readily change their hue ; and not only the tone of the general background but its colour-pattern may be simulated with great fidelity by certain teleostean fishes. The most remarkable changes of this type are seen in the groupers (Epiriephelus) that swim over the variegated patterns of the coral reefs in tropical waters and within a few minutes may change a livery of bright blues and browns into an equally brilliant costume of yellow and black ; a similar virtuosity is seen in flat-fishes such as the fiounder, Paralichthys albiguttus (Kuntz, 1916 ; Mast, 1916). It is interesting that adaptation during the early stages of development may play an important part in determining the final pattern of colour in the adult ; thus if the larvae of the crested newt, Triturus cristatus, develop on a dark background the yellow markings of the adult become suppressed, if on a light background, the dark markings suffer a similar fate (Lautz, 1953). It is to be noted that all these reactions are completely dependent on the eyes and have invariably been shown to be lost if the animal is blinded or even if it is dazzled by a blinding light which abolishes the contrast between the dorsal and ventral portions of the retina (octopus. Prince, 1949). (c) Occasionally indirect responses may follow stimulation of receptor mechanisms other than the eyes — the mid-brain as in some fishes {Phoxinus — Scharrer, 1928) or the pineal body as in lampern larvae (Young, 1935) or teleostean fishes (Breder and Rasquin, 1950). AmmoccEte larva of lamprey The central organization of these pigmentary changes is as varied and complex as the variations in the colours themselves, and in view of the multiplicity of the types of chromatophores and their reactions it is not surprising that our knowledge of their control is by no means complete in spite of much research. Apart from local primary reactions, two methods of coordination are found, hormonal and nervous, the first the more primitive and slower in its development, the second the more elaborate and efficient. Sometimes the one is present alone, as is seen, on the one hand, in the simple hormonal control found in Crustaceans, the more primitive Fishes, frogs and lizards, or, on the other hand, in the simple nervous control found in the leech or the chameleon. More often the two are combined in a dual mechanism of coordination, the hormonal control being sometimes the preponderatiiig influence as in Insects or the eel, but usually being 1 Portunus — Abramowitz (lOST)) ; Planes — Hitchcock (1941). ■ Sepia— Kiihri and Heberdey (lSt29), Kuhn (1950). LIGHT AND PIGMENTATION 93 dominated by the nervous mechanism as in Gephalopods such as the octopus or the more highly developed Teleosteans such as the cat- fish. The hormones {chroniatophorotropins), of which there may be more than one with mutually antagonistic reactions, are elaborated in Crustaceans in the neuro -secretory cells formed in the eye-stalks and elsewhere in the central nervous system ^ ; in Vertebrates the pituitary- hypothalamic complex ^ is the primary source although the adrenals may provide an antagonistic element. The nerve supply may be simple with one tj^^je of fibre which is pigment -concentrating as in the dogfish or the chameleon, or it may be dual comprised of two opposing types of fibre, one resembling adrenalin with a pigment-concentrating (symjDathetic) action being antagonized by a second resembling acetyl- choline with a pigment-dispersing (parasympathetic) effect. Among ANNELIDS, such as some polychsete worms (Hempelmann, 1939) and leeches (Wells, 1932 ; Janzen, 1932 ; Smith, 1942), most of which become pale in darkness and dark when illuminated, the evidence suggests that the control is primarily nervous, correlated most effec- tively through the ocelli at the anterior end but operated less efficiently by widely distributed photoreceptors through segmental reflexes. Thus if a leech is decapitated or stimulated faradically, a pale animal kept in darkness will become pigmented, but if the nerve-cord is truncated the change passes only to the level of trans- section ; while decapitated animals show the same responses as normal animals but respond more sluggishly (Smith, 1942). Among these animals there is no evidence of a response to the background. In CEPHALOPODS there is a slowly acting hormonal control, probably mediated by substances of the nature of tyramine and betaine ; the former has an adrenalin -like action increasing the tonus of motor centres and producing a dark coloration, while the latter, like acetylcholine, decreases the tone of the chromatophores and lightens the animal. The injection of these substances produces the same colour changes as also does the transference of blood from a dark to a light animal (Sereni, 1928-30). This simple and fundamental chemical action, however, is dominated by nervous activity ; the stimulus is received primarily through the eyes, control being maintained through centres in the cerebral and suboesophageal ganglia, the isolation of which by nerve section stops all colour change in the area affected, and the response is effected probably by a double innervation, both excitatory and inhibitory, to the muscles of the chromatophores (Phisahxi 1892-94 ; Sereni, 1927-28 ; Bozler, 1928-29). Among INSECTS the control is both hormonal and nervous and the part played by the eyes varies. In this respect the stick-insect, Dixippus, has been investigated most extensively (Giersberg, 1928). ' p. .').52. - p. 556. Leech ]!ephalopod (Octopus) 94 THE EYE IN EVOLUTION In it, the eyes are the sole photoreceiDtors and their occhision or section of the optic tracts inhibits all normal responses (Atzler, 1930) ; but the fundamental role of hormonal control is seen in the fact that transplanted portions of integument react normally long before nervous connection can be established (Janda, 1936). On the other hand, in the grasshopper, Acrida turrita, some colour changes (adaptation to red, orange, yellow and violet) are said to occur after the eyes are totally varnished, while a green colour can be developed only if the eyes are functioning (Ergene, 1952). Among CRUSTACEANS the vividly dramatic colour changes are '•:2?* I' *r' / 4 -Colour Changes in Crustaceans. The three shrimps (Crago) were initially coloured alike, as the specimen on the left. This was used as a conti'ol and showed no change after an injection of sea-water. That in the centre was injected with an alcohol-insoluble fraction of the commissures ; that on the right by a total water-soluble fraction of the commissures (Brown and Klotz). Prawn entirely mediated by hormones elaborated in the cephalic neuro- secretory system. 1 That a blood-borne agent was the responsible factor was first demonstrated by Roller (1925-30) who found that the colour of a lightly coloured shrimp, Crago vulgaris, could be altered by blood transfusion from a darkened specimen. Perkins (1928-32) thereafter discovered in the prawn, Pakemonefes, that denervation of a region had no effect on colour responses while occlusion of the blood supply inhibited them ; he also demonstrated that injection of an extract of the sinus gland induced blanching in a blinded animal while removal of the eye-stalks resulted in the assumption of a permanently darkened appearance. These early results have been amply confirmed and it would appear that the intricate control of the chromatophores of Crustaceans is effected by at least two and sometimes three or four ^ See further p. 554. LIGHT AND PIGMENTATION 95 chromatophorotropiiis antagonizing and supplementing each other, neither species- nor genus -specific, secreted in various jjarts of the neuro-secretory system ^ (Fig. 08). In some cases the process is more complex and adaptation to the background is achieved by the produc- tion of different hormones when the dorsal or the ventral aspect of the retina is stimulated (the Isopod, Ligia oceana — Smith, 1938). In CYCLOSTOMES and the more primitive fishes such as the SELACHIANS - liomiones derived from the pituitary seem to be the only active agents in the control of the chromatophores, a pigment- Ligia Sun ^^ Background Fig. 69. — The Controlling Mechanism of the JMelanophores of a Fish (the Eel, Asouilla). The direct light from the suti strikes the ventral portion of the retina, VR, while the light reflected from the background strikes the dorsal portion, DR. From the retina nerve paths lead to the central nervous system, CNS, and thence directly to the chromatophores by adrenergic nerve fibres, AN, and cholinergic nerve fibres, CN. A second relay is made to the pituitary body. Pit, from which hormones are flistributed through the lilood vessels, BV. CM is a chromatophore with its melanin concentrated ; DM with its melanin dispersed (after Parker). dispersing agent (intermedin) causing darkening and a pigment- concentrating factor causing blanching ; the colour of the fish is determined by the ratio of these two antagonistic substances in the blood, this ratio being in turn controlled by visual stimuli through the differential effects of dorsal and central stimulation of the retina (Zondek and Krohn, 1932 ; Lundstrom and Bard, 1932 ; Young, 1 The shrimps, Crago and Pala'inon, the fiddler crab of the Pacific coast of N. America, Uca, the lobster, Homarus, etc. (Hanstrom, 1933-35 ; Brown and his colleagues, 1933-52 ; Webb et ah. 1951). ^ Cyclostomes, such as the lamprey, Lampeira — Young (1935) ; Selachians, such as the skate, liaja — Parker (1937), and the dog-fish, Scyllium — Young (1933). 96 THE EYE IN EVOLUTION Anguilla 1935 ; Hogben, 1936). In teleostean fishes, however, which show more elaborate colour changes than any other species, a dual mechanism emerges for a more efficient nervous control has developed, depending on the excitability of specialized retinal areas above and below the level of the optic nerve (Hogben and Landgrebe, 1940) (Fig. 69). In some types, it is true, the hormonal influence remains preponderant ; this is seen in the eel, Anguilla (Neill, 1940 ; Waring, 1940), or in the minnow. Fig. 70. — Colour Changes in the Female Clppy, Ljmisr^s kejiculatus On the left the noi'mal aninial ; on the right a fish after 25 /Lig. per ml. of LSD (D-lysergic diethvlamide) had been added to the water of the aquarium (Sancloz J. Med. Sci., 1956). Figs. 71 and 72. — The Melanophores of the Guppy, Lubistux itmicnLATL {SandozJ. Med. Sci., 1956). J^^"^^*- .*? *'>".<*f«.?j Fig. 71. — After adaptation to a light environment. Fig. 72.— After LSD (25 /xg. per ml.) had been added to the water of the aquarium. Mustelus Phoxinus Icevis, in which even section of the sjDuial cord fails to alter the response to the background (Healey, 1951-54 ; Gray, 1956). In most Teleosteans, however, colour changes are dominated by a nervous control which persists in hypophysectomized animals. That the changes in the chromatophores were determined by chemical mediators liberated at the nerve terminals has been shown in a striking series of experiments by Parker (1940-55), who studied the effects of sectioning the radial nerves of the tail-fin. The chromatophores of Selachians possess a single innervation mediated by an adrenalin-like substance, selachine, which is pigment -concentrating (the dogfishes, Mustelus and LIGHT AND PIGMENTATION 97 Squalus — Parker, 1935-36) ; Teleosteans possess a double innervation with, in addition, pigment -dispersing fibres the action of which is mediated by acetylchoHne (the kilhfish, Fundulus — Parker, 1934 ; the catfish, Ameitirus — Mills, 1932, Parker, 1940-41 ; and other Squalus species). These two types of nerve correspond to the sympathetic and parasympathetic systems of warm-blooded animals since adrenalin blanches and acetylcholine darkens the eserinized animal (Giersberg, 1930 ; Smith, 1931). Similarly, darkening of certain Teleosts (the giippy, Lebistes reticulatus) can be brought about by adding D-lysergic Ameiurus acid diethylamide to the water of the aciuarium (Cerletti and Berde, 1955) (Figs. 70 to 72). At the same time, however, even in these Fig. 73. — The Effect of the Injection of Pituitrin on a Frog. The right animal injected six hours previously witli pituitary extract from a fietal ox ; left, control (Hogben). fishes some hormonal influence remains since pituitary extracts are slowly efi:ective in denervated areas (Matthews, 1933 ; Kleinholz. 1935 ; Abramowitz. 1937). AMPHIBIANS were the first class of animals in which a humoral control of colour was demonstrated, when P. E. Smith (1916) showed that hypophysectomized tadpoles remain indefinitely pale. Although there is some evidence of a mmor nervous influence in some species such as the darkening of the leg of the toad, Bufo arenarwn, on section of the sciatic nerve and its blanching on peripheral stimulation of the cut nerve (Stoppani, 1942). it may be said in general that amphibian chromatophores are essentially under humoral control. This is main- tained by two antagonistic hormones elaborated in the pituitary- hypothalamic system — a melanin-concentrating W-snbstance causing Bufo S.O. — VOL. I. 98 THE EYE IN EVOLUTION Rana Xenopus Anal is Phrynosoma blanching, mediated by the pars tuberahs, and a melanin-dispersing B-stibstance (intermedin) mediated by the posterior or intermediate lobe ; their relative concentration in the blood is determined by environmental stimuli operating through the eyes and their activity is usually abolished when these or the optic nerves are destroyed, although some residual responses remain after removal of both eyes which may be due to the direct action of light on the hypothalamic region (Rowlands, 1952-54). These conclusions have been confirmed by the effects of excision of the whole or parts of the pituitary and by the induction of colour changes by the injection of extracts of the gland both in the frog, Raiia} and in the African clawed toad, Xenopus Icevis - (Fig. 73). It is also interesting that injection of pineal extract produces a contraction of the melanophores of Xenopus (Bors and Ralston, 1951) while pigmentary changes are constantly produced in tadpoles by feeding on pineal tissue (McCord and Allen, 1917). REPTILES, like Aniijhibians, show less elaborate responses to light than teleostean Fishes ; the only conspicuous changes occur among lizards and the only active cells are the melanophores which send up pigment into their branches entwined among the variegated chromato- phores, thus varying the colour scheme ; the gaiety of their various costumes is due to individual variation in these static cells. The only phdtic response is to light entering the eye, and the colour of the background is without primary significance. Within these limitations, however, the large family of lizards shows every possible variation in control. On the one hand, the iguanid, Anolis (the " Florida chameleon "), shows little evidence of nervous intervention ; it becomes dark brown in bright illumination, pale green in darkness ; a hypophysectomized or a blinded animal becomes light green and thereafter loses all colour responses except a peculiar mottling on electrical stimulation or on the injection of adrenalin ; while denervated areas of the skin respond as do normal areas (Kleinholz, 1938) (Figs. 62 and 63). An intermediate position is occupied by such iguanids as the American horned "toad," Phrynosoma. The chromatophores of this animal are under the influence of pigment-concentrating nerve fibres and react to adrenalin ; stimulation or section of these fibres results respectively in blanching or abolition of responses. At the same time the injection of pituitrin or of the blood of a darkened specimen induces darkening, while hypophysectomy or the injection of adrenalin, adrenal extract or of blood from a pale animal induces blanching (Redfield, 1918 ; Parker, 1938). It would seem that the two antago- nistic hormones act directly on the chromatophores since they are 1 Hogben and Winton (1922-23), Steggerda and Soderwall (1939), Parker and Scatterty'(1937). 2 Hogben and Slome (1931-36), Atwell and Holley (1936). LIGHT AND PIGMENTATION 99 equally effective in areas denervated by nerve section. On the other hand, in the chameleon the chromatophores show no evidence of hormonal control and appear, apart from the primary response characteristic of this animal, to be influenced solely by one set of pigment-concentrating nerves ; denervation results in darkening, possibly due to the absence of tonic impulses, whereafter there is a complete absence of further responses (Hogben and Mirvish, 1928 ; Zoond and Eyre, 1934 ; Sand, 1935). Abramowitz. Proc. nat. Acad. Sci., 21, 677 (1935). Biol. Bull., 73, 134 (1937). Armstrong. Bird Display and Behaviour, London (1947). At well and Hollev. J. c.vp. ZooL, 73, :^3 (1936). Atzler. Z. vergl. Physiol., 13, oU5 (1930). Babak. Pflitgers Arch. ges. Physiol., 149, 462 (1913). Bauer. Z. allg. Physiol., 16, 191 (1914). Bors and Ralston. Proc. Sac. exp. Biol. Med., 77, 807 (1951). Bozler. Z. vergl. Physiol., 7, 379 (1928) ; 8, 371 (1929). Brecher. Arch. EntuMech. Org., 50, 41 (1922). BrederandRasquin.6'fience,lll, 10(1950). Bristowe. 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B, 112, 228 (1933). Quart. J. micr. Sci., 75, 571 (1933). J. e.vp. Biol., 12, 254 (1935). Zondek and Krohn. Klin. W.ichr., 11, 405 (1932). Zoond and Eyre. Philo.s. Trans. B, 223, 27 (1934). CHAPTER V THE EMERGENCE OF VISION In the varying reactions of living organisms to light that we have now studied, in some cases vision does not — or need not — co-exist, in others an associated sensory impression is conjectural and unimportant while in others it seems to be a necessary accompaniment ; indeed, it is no easy matter to decide where its origin lay or when the sense of vision first became a factor in conscious behaviour. There are many creatures which have no eyes (as we understand the term) and yet " see " (using the word in its widest sense) ; and equally reasonably it may be said that there are many which have what we may well call " eyes " and yet see not. To a considerable extent the matter is one of definition ; on the one hand, few would acquiesce with Max Schultze (1868) who spoke of the transformation of luminous into nervous energy as vision ; more would agree with Hesse (1908) who contended that the light-sensitiveness of primitive creatures did not imply the possession of a light sense. On the other hand, there are those w^ho would ascribe to all animals which react to light a sentiency, no matter how vague (McDougall, 1933). To many this may seem gratuitously anthropocentric ; for if such an awareness, tinged with affective tone, is ascribed to the amoeba as it flees from a bright light and expands in mid-intensities of illumination, is it to be ascribed also to the speedwell which opens its petals to the mid-morning sun? The question is disputable ; but whichever attitude we adopt the most illegitimate premise from which we can reason is the assumption that an organism has the same appreciation of light and patterns of shade or hue as ourselves, whether it reacts diffusely without specific end-organs or whether it is possessed of eyes more highly differentiated for the resolution of visual images than the relatively simple eyes of man.^ It must be remembered, however, that vision is one of the latest senses to be evolved and that in its phylogenetic development it lingered long behind those depending on mechano -receptors and chemo-receptors. Even when a considerable stage of complexity had been reached there was little attempt at discrimination ; for this purpose reliance was placed upon those senses which are more fully developed in primitive life — the tactile sense, the chemical sense, and the olfactory sense. The great majority of animals are non-visual ' The few sicjn-stimuli to which the vision even of birds is limited are striking examples (p. 664 , THE EMERGENCE OF VISION 103 creatures depending essentially in their behaviour on non-visual stimuli. For example, the scallop has numerous visual cells around the edge of its mantle, and if these are stimulated by the " sight " of its enemy, the starfish, no response except the awareness of the presence of something is elicited, and no attempt at flight is made ; but whenever some extract of starfish is added to the water in which the animal lies, the scallop immediately runs away (Dakin, 1909 ; von Uexkiill, 1921). ]\Ioreover, in Pecten, no response is called forth until the object moves, and any movement of any object excites the same response, a protrusion of the tentacles ; these are endowed with organs of Fig. 74. — The Sensory Reactions of the Water Beetle. A watery meat extract is contained in tiie bag. The feeding responses of Dytiscus marginalis show its dependence on chemical stimuli rather than vi.sual (Tinbergen, Study of Instinct ; Clarendon Press). chemical and tactile sensitivity which exjilore the object " intelligently", and on the results of their findings the animal either eats or flees (Dakin, 1910). The purpose of this response is obviously to secure further information in a form in which it is analysable. Even in man the olfactory sense organs are relatively more fully developed than the visual at birth ; a fish with its olfactory nerves severed ceases to feed spontaneously (Steiner, 1888) ; and the lately-born rabbit will die of starvation if deprived of the sense of smell because it cannot find the teats of its mother, even although it has been allowed to make use of its eyes before it has suffired the loss of the more fundamental sense. 104 THE EYE IN EVOLUTION It must also be remembered that even although vision is well developed it may not be used in many innate reactions for the efficient execution of which it would appear to us to be of value. The feeding response of the carnivorous water-beetle, Dytiscus marginalis, is a good example of this (Tinbergen, 1936) (Fig. 74). This beetle has elaborately developed compound eyes and can be trained to respond to visual stimuli. Its feeding response, however, is released only by chemical and tactile stimuli, and visual impressions, even those of a moving prey, never release this reaction. Thus in the presence of a watery meat extract it neglects the source but, going to the region of highest concentration, it attacks any solid object it touches. Of the three fundamental effects of hght on Hving organisms — the stimulation (or occasionally the depression) of metabolic activity, the orientation of movement, and the control of pigment and colour — it would he reasonable to assume that the first, equally shared between plants and animals, does not necessarily involve vision as a conscious experience, occurring as it does in Protozoa and eyeless types. ^ In its more primitive form this activity may conjecturally be accompanied by a vague sentiency, but this can be little more than an awareness of light, and even in its most advanced forms it is essentially a chemical or hormonal function for the implementation of which eyes are effective but not unique receptors. The last — the control of colour — is a late evolutionary development, and although j^oikilochromic reactions would appear to occur without conscious accompaniment, in their higher developments they would seem to imply the existence of a visual sense in the organism for whose benefit (or confusion) they are intended. The economy would seem unnatural and contrary to all biological trends that at one time urged all plants except the modest Cryptogams, in their struggle for existence in a cooling world, to luxuriate so shame- lessly in the blatant sexual exhibitionism of flowering if the pollinating insects could not both see and appreciate their charms ; their appre- ciation, however, has probably no resemblance to the interpretation of the same imagery by the human brain. Equally uneconomic would be the scandalously attractive dress put on by many fishes and birds for tlieir love-making. Clearly, if they are endowed with biological usefulness and survival-values, allsesthetic characters — and without these endowments they would not jiersist — must be appreciated by other organisms. Although the eyes serve as the receptors for many adaptive colour changes, this function need not imj^ly that the animal it'self has any conscious appreciation excited by shifting visual patterns. Even when the responses are mediated nervously and are rapid and complex, as in teleostean fishes, they show no parallelism with what is known of the visual functions of the animals concerned, for reflex alterations of the chromatophores may occur to suit differences in shade of the back- ' Such, for example, as the white cave crayfish, Cambarus ayersii (Wells, 1952). THE EMERGENCE OF VISION 105 ground too small to excite visual discrimination in training experiments. Many of the reactions, as we have seen, are hormonal ; some may occur in eyeless animals ; and indeed, in species wherein these organs are necessary for their occurrence the chromatophores may still respond if the eyes are transplanted to a new location in the body (as was demonstrated in the adult fish, Fitzroya lineafa, by Szepsenwol, 1938). Temperature and humidity, as seen in Amj)hibians and Reptiles, may be equallj^ or more effective stimulants in comparison with light, and although heat and light usually coincide in natural surroundings, the paling of the desert lizard in the heat of noon so that it blends with the sand is fortuitous so far as its own vision is concerned. Tactile organs are sometimes adequate receptors as is seen in the control of chromato- phores by the suckers of Cephalopods (Steinach, 1901) ; while the adoption of a brown colour by the European tree-frog, Hyla arborea, when it steps on a rough surface and of a green colour on a smooth surface brings about an environmental adaptation to a background of tree-bark or leaves respectively as adequate as any photic response. Indeed, many of these colour reactions are fortuitous so far as adapta- tion to a background is concerned ; thus the iguanid lizard, Anolis, turns green in the shade and brown when exposed to light, and it is merely coincidental that in its natural haiuits it usually becomes invisible on a background of shady foliage in the first event or of soil in the second, since, if it is removed from the shade upon a green leaf and placed in the sun still sitting on the leaf, it promptly changes its colour into a vividly contrasting brown (Wilson, 1939). It is essentially from the primitive motor response to light that vision almost certainly developed. In natural circumstances these tropisms and taxes are invariably of biological utility, and it would appear that the essential and 'primary function of vision was the control of movement iyi order to attain an optimum environment as efficiently as jiossible, a function which is eventually employed for the avoidance of obstacles, the pursuit of prey and flight from enemies, and survives in man in the close relationship between the eyes and the vestibular apparatus and in their importance in the control of posture. It follows that visual organs are found almost solely in actively moving animals, while in such as assume a sedentary phase they tend to degenerate and disappear.^ The stage at which these motorial responses to light evolved beyond purely reflex acts below the level of consciousness and became endowecl with awareness is impossible to conjecture. This question has given rise to a controversy which is still luisettled. In the simple philosophy of Aristotle - and for 2,000 years thereafter no argument arose ; plants had a vegetative soul responsible for growth and repro- 1 o. 721. - p. 28. 106 THE EYE IN EVOLUTION duction, to animals was added a sensitive soul governing movement and sensation, and to man a rational soul. But doubts occupied men's minds particularly in the seventeenth and eighteenth centuries in the long disputation between the materialistic French Cartesians who followed Descartes (1596-1650) and the English Newtonians who were inspired by Newton (1642-1727) on the one hand, and the mystic German Nature-philosophers on the other, the disciples of Paracelsus in the classical tradition, who found philosophical expression in Leibnitz (1646-1716) and Goethe (1749-1832). To the first the universe was essenti- ally mechanical ; to the second not only living creatures but minerals and chemical compounds were permeated by a directive vital force. A middle view was represented by Lamarck (1744-1829) who claimed that the lowest organisms were insensitive and that their conduct was completely governed by external factors, driving forces derived from the environment ; but as the evolutionary scale was ascended and a centralized nervous system was acquired, organisms generated their own " sentient interieur " to a progressivly greater degree, thus attaining an ever-increasing measure of self-determination until Vertebrates were reached, at which stage intelligence became possible and ultimately found its fullest expression in Man. Each of these views has been maintained in recent times — the simple reflexology represented by Loeb (1918) and the Russian school (Sechenov, 1863 ; Bekhterev, 1913 ; Pavlov, 1926-27) on the one hand, and the purposive or "directive" psychology represented by Whitehead (1929), McDovigall (1933) and Russell (1934-45) on the other, wherein vital force has been replaced by the " general drive " of modern biologists, a state of tension or action-energy which activates living organisms. Each view would find its advocates today. The mechanistic view would place the emergence of visual reflexes into the plane of consciousness as a late development. This attitude found its apostle in Jacques Loeb (1906-18) ^ who considered that all the orientating and instinctive reactions of the lower animals to light or other stimuli were mechanically determined ; although in many- cases it seems to respond voluntarily and often purposively, the move- ments of the phototactic animal are those of a robot ; it is forced to go where it is taken by its reflexly-driven cilia, legs or wings, an activity in which consciousness or vision has no place. Even an ant with all its proverbial intelligence orientates its journey to light unthinkingly as does a sleep-walker or an automaton ^ and in this respect is as unteach- able as a machine, completely totalitarian and incapable of individual adjustment. It must be remembered that the new science of cybernetics has demonstrated that similar reactions, sometimes of astonishing complexity, can be carried out by non -vital mechanisms, those curious electro -mechanical first cousins of computing machines, which by a combination of photo-cells, amplifiers, motors and automatic governing devices, can simulate many of the reactions of living things, not in appearance bvit in behaviour, as they navigate themselves around the play-room of the electronic engineer (see Ashby, 1952 ; Walter, 1953 ; and others). Such mock-biological robots, goal-seeking and self-regulatory, capable of the storage of information and possessed of a rudimentary type of memory 1 p. 28. 2 p (38_ THE EMERGENCE OF VISION 107 maintained by electrical oscillations, have been constructed so that they can explore their environment with an apparent purpose. A photo-cell can serve as a receptor and amplifiers and motors can be interconnected in such a way that a positive taxis (for example) to a moderate light and a negative taxis to bright light (or to material obstacles, gradients, etc.) can endow it with the faculty to discriminate between effective and ineffective behaviour, to seek actively an environment with moderate and optimal conditions, to acquire conditioned reflexes, and even to perpetuate its activity and " feed " itself with electricity by being optically attracted to a charging circuit when its batteries begin to fail. On the other hand, there are those who consider that such auto- mata have httle resemblance to even the simplest living things ; their behaviour has only a superficial appearance of being dominated by- taxes and kineses, by memory, habituation or trial-and-error learning. The school of biological philosophy formalized by Whitehead (1929), amplified by McDougall (1933) and pursued by such recent writers as Agar (1943) and Thorpe (1956) argues that every vital event is an act of percejition. a mental as opposed to a material process ; a living organism is essentially something which perceives ; its behaviour is not an automatic response to sensory impressions but includes an element of purpose building up primary perceptions into unitary systems in which the whole is different from and greater than the sum of its constituent parts. Such a view, as we have already hinted, tends to pan-psychism, or even to pan-theism ; according to it a purely objective biology is sterile ; like the warp and woof, mechanism must be interwoven with teleology.^ While mechanisms may even- tually become explicable in physico-mathematical terms, there is no suggestion yet that the subjective concepts of conscious purpose ever will be (Sommerhoff, 1950). But. even although this is agreed, it is to be remembered that there are no grounds for supposing that any well-defined mental content is associated with the reactions of the lower animals comparable to the perceptual experiences of the higher animals. On tlie whole it would seem that the matter is not so simple as the more materialistic outlook might suggest. It is true that many of these primitive tropic activities of the animal world can be interpreted as reflexes without motivation, incentive or appreciation ; but because there are no discernible conscious acconipaniments to many purely reflex acts in man whose apperceptive powers have been translated from the level of ganglia to the cerebral cortex, it by no means follows that there are none in those lowlier organisms the nervous system of which consists only of ganglia and nerve -fibres — or even of an un- centralized nerve-net or nothing at all. It must be remembered that the transference of sensory appreciation to the neopallium occurred late in evolutionary history,^ and that although the lower centres in man have 1 See D'Arcy Thompson (1942). = p. 542. 108 THE EYE IN EVOLUTION become merely relay-stations in this respect, they used to subserve much more important functions. Indeed, in the higher animals — and to some extent also in man — much of mental and most of visual activity, especially those aspects associated with primitive responses and endowed with emotional tone, remain closely associated with the vegetative activities which are integrated in the thalamus. Even in Fishes and Amphibians, vision is entirely unrepresented in the cortex. Thus although ablation of his occipital lobes deprives man permanently and completely of all sensations of light, the higher mammals are by no means so incapacitated. 1 Most decerebrate Vertebrates will react and exhibit emotions to visual stimuli and even perform complex instinctive reactions without difficulty. So will the headless bee sting with accuracy on irritation (Bethe, 1897) and the clover-fly clean its wings with its legs after decapitation (Sherrington, 1920). A brain, or even a head -ganglion, is thus not a necessary residence for apparently " intelligent " reactions. Phototactic reactions are " instincts", that is, adapted reactions of a purposive nature handed down from the previous experience of ancestors ; and, as with all instincts, the component afferent impulses have become associated in consciousness and synthesized into a meaningful pattern, a process which necessarily connotes some degree of perception. 2 As instincts, their usual stereotyped uniformity can be modified by experience provided the modification tends to the well- being of the individual — or the race. The reactions of even the lowly earthworm are amenable to training ^ ; many molluscs are readily trainable ; many insects eminently so. Thus the photo -negative cockroach, BlateUa gennanica, can be conditioned to advance towards a light provided it has been taught that a dark and comfortable shelter is placed beneath it (Goustard, 1948). Similarly, as we have seen,* after interference with its receptors or effectors either by partial blinding or by removing some of its legs, the mutilated insect will rapidly modify its reactions and after several trials will learn to orientate itself to light with almost the same accuracy as before. It is thus impossible to say where in the animal scale reactions to light were first associated with conscious awareness ; nor can we guess the form such consciousness may take, for like a solid to an inhabitant of Flatland, it exists in a form which cannot be assessed by the measuring instruments at our disposal ; we can only reason by inference from an analysis of our own peculiar form of consciousness of which alone we have immediate knowledge. From a study of the sensory capacities of animals few things emerge more certainly than that each species has its own perceptual world (the MerhveU of v. Uexkiill, 1921), and that 1 p. 545. 2 See Lloyd Morgan (1896-1912), Jennings (1906), Sherrington (1920), Parsons (1927), and manv others. » p. 573. " « p. 59. THE EMERGENCE OF VISION 109 each of this midtitiide of worlds bears Httle resemblance to the environ- ment of the animal as we see it or interpret it in terms of our own Merkwelt. It seems reasonable to assume that the development of vision as a facet of consciousness evolved in three stages. We may surmise that the first conscious appreciation was a mere sentiency, crudely vague and undifferentiated, characterized perhaps by a minimum of cognition endowed with a rudimentary affective tone ; it was limited perhaps to an awareness of the existence of light as a change in the environment, tinged perhaps with sufficient affective tone to allow it to be appreciated as pleasant or mipleasant, and endowed witli meaning in so far as the organism responded apjDropriately by motor activity in which initially there was offered the choice only of two alternatives, towards or away from the source of stimulation. We may even surmise^ as indeed exjjeri- mental evidence on the amoeba would suggest,^ that the most primitive sensation was a co-sesthesis without constituent modalities in which the several senses as we know them were merged into a vague and indis- criminate unity, and the stimuli (photic, chemical, tactile, etc.) which to us are distinct and unrelated were co-equal and additive. Some such concept as the emergence of a consciousness of a lowly type at an early but unknown stage, on the reflex plane or even below, would seem a possible hypothesis, a consciousness at first indefinable and vague but at the same time sufficiently plastic to contain the germ of the elaborate emotional behaviour of the higher animals — so long as we remember that the latter with all its undoubted richness and com- plexity bears little resemblance to the consciousness of man. For such a surmise, however, there is no direct evidence; at this level the motor response to stimulation is all we can directly assess. From morphological and behavioural observations, however, we can be more certain that a primitive perception of light emerged with the development of a centralized nervous system in worms - ; at this stage in evolution it would seem reasonable to suppose that a mechanism became available for the creation of perceptual symbolism; and at this stage vision undoubtedly became a perceptual process forming part of the conscious life of the animal and capable, at first in a minor degree, of determining its conduct. As we ascend the animal scale the primitive light-sense evolved into a sense of appreciation of the directional incidence of light, of movement, of form, and eventually of colour, until in the Primates the capacity to analyse complex visual patterns ])ecame the chief determinant of conduct. In its final development, the first elements of which have been detected in the chimpanzee,'* the sense of vision j^assed beyond the stage of passively 1 p. 3G. Compari' also the integration of jjliototaxi.s and galvaiiotroi^ism seen in certain worms (p. 33). ^ p. 572. ^ p. 602. 110 THE EYE IN EVOLUTION recording objective appearances in the outside world and emerged as an imaginative and creative sense. This aesthetic quahty was certainly a late acquisition acquiring maturity only in man.^ The extent to which in the animal scale an appreciation of these three progressive stages became a factor in the customary activities of the life of living organisms is a question which must await the acquisition of a much more profound knowledge of their natural history than we at present possess. And — whatever the future may bring forth — the manner of its becoming so is inexj^licable by any physico-mathematical techniques we have at our disposal today or will have tomorrow. Agar. 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The Behaviour of Animals, London (1934). The Directiveness of Organic Activities, Cantab. (1945). Schultze. Untersuch. il. das Zusam. Auge der Krebse u. Insekten, Bonn (1868). Sechenov^ The Reflexes of the Brain (1863) : Trans, in Selected Works, Moscow (1935). Sherrington. Tlie Integrative Action of the Nervous System, Yale (1920). Sommerhoff. Ancdytical Biology, Oxon. (1950). Steinach. Pfliigers Arch. ges. Physiol., 81, 1 (1901). Steiner. Die Functionen des Central- nervensystem, 2 (1888). Szepsenwol. C. R. Soc. Biol. (Paris), 129, 1265 (1938). Thompson, D'Arcy. On Growth and Form, Cantab. (1942). Thorpe. Learning and Instinct in Animals, London (1956). Tinbergen. De Levende Natuur, 41, 225 (1936). von Uexktill. Umwelt u. Innenwelt der Tiere, Berlin (1921). Walter. The Living Brain, London (1953). Wells. Anat. Rec, 113, 613 (1952). Whitehead. Process and Reality, Cantab. (1929). Wilson. Amer. Nat.. 73. 190 (1939). p. 753. PART II THE EVOLUTION OF THE VISUAL APPARATUS The Morphology of Invertebrate Eyes The Systematic Anatomy of Invertebrate Eyes The Eyes of Protochordates The Evolution of the Vertebrate Eye The Eyes of Cyclostomes The Eyes of Fishes The Eyes of Amphibians The Eyes of Reptiles The Eyes of Birds The Eyes of Mammals The Central Organization of Vision Fig. 75.— Richard Hesse (1868-1944). CHAPTER VI THE MORPHOLOGY OF INVERTEBRATE EYES RICHARD HESSE (1868-1944) (Fig. 75), one of the greatest of German zoologists, probably contributed more towards the study of the sense organs, particularly the visual organs, of the lower animals than any other single indivi- dual. The greater part of his life was devoted to this subject. Professor of Zoology at Tiibingen in 1901, he became Professor at the Agricultural School in Berlin in 1909, occupied the Chair of Zoology at Bonn in 1914, and was Professor of Zoology and Director of the Zoological Institute at the University of Berlin from 1926 to 1935. His systematic study of the light-sensitive organs of Invertebrates was lai-gely conducted between 1896 and 1908 and included an immense range of types varying from the relatively simple eyes of worms to the highly developed visual organs of Molluscs and Arthropods, an interest which he maintained throughout his long and' fruitful life. As will be seen in the following pages, his studies form the basis of our understanding of the astonishing variation in the morjDhology of the eyes of the Invertebrates. It is surprising how little systematic work has been done on this fascinating subject since his day. THE GENESIS OF THE EYE It is evident from the subject-matter of the previous chapters that the eye has evolved from remote and lowly origins, far removed in form and in function from the highly specialized mechanism we find in Man. In the most primitive miicellular organism, as we have already seen in the case of the amoeba,^ there is a diffuse reaction to light whereby the entire cell, and particularly its superficial layers, in the absence of any apparent specialization of structure responds by a simple alteration of the sol-gel reversibility of the relatively fluid protoplasm. In its earliest form this would seem to be an imdifferentiated response common to all stimuli (photic, tactile, thermal, chemical) (Pantin, 1924-26 ; Folger, 1926-27 ; Mast, 1926-32). A reaction of this simple nature to light is t\^3ical of the Rhizopods, such as the amoeba, but among multicellular organisms we would expect it to be localized preferentially in the cells on the surface which are exposed to the stimuli of the external world ; it thus evolves into a general dermal jihotosensitivity. This may occur sometimes in the absence of known photoreceptors, sometimes in association with them, and it is interesting that even when these are present, the more primitive and less specialized mechanism may dominate the behaviour of the animal in its reactions to light more effectively than the conspicuous receptor organs. 1 p. 3.-,. 114 THE EYE IN EVOLUTION Dytiscus Myxine A nodonta The mechanism of this dermal sensitivity is conjectural. The reaction may be initiated by photosensitive pigments and, although in most cases such have not been identified, they could be present in very small amounts (von Uexkiill, 1897). On the other hand, it is conceiv- able that nerve elements lying subdermally may be directly stimulated, a view for which Millott (1954-57) produced firm evidence in the case of the sea-urchin, Diadema. Such a reaction would correspond to the activity of the organelle of the apolar hght-sensitive cells of worms, the sixth abdominal ganglion of crayfish and lobsters,^ and the nerve elements in the diencephalon of lampreys, minnows and ducks. ^ Again, Bohn (1940) and Viaud (1948) looked upon the reaction as a common property of protoplasm depending on " electrochemical polarization", a property readily evident in lower forms but often neutralized or masked by more potent reactions in higher forms. Such a dermal light-sensitivity (the dermatopsia of Graber, 1884) is of wide distribution occurring in members of almost all phyla. ^ While it is usually diffuse it may be particularly well developed in certain situations wherein its biological utility is greatest, often the fore-pai't of the animal or in such situations as the region of the spiracles of the abdomen of the larv.'B of the water-beetles, Acilius and Dytiscus (Schone, 1951). Such a sensitivity is particularly marked and widesj^read among Echinoderms (Cuenot, 1891) ; it occurs in some Molluscs, Turbellarians and Annelids, as well as in some Insects, in Cyclostomes [Myxine glutinosa, Newth and Ross, 1955), in eyeless cave-fish (Thines and Kahling, 1957) and in blinded cat-fish. The response to dermal sensitivity is, of course, a photo- kinesis which may be either jjositive or negative. Thus the eyeless mussel, Anodonta, reacts to a passing shadow (Knoop, 1954 ; Braun and Faust, 1954), blind cavernicolous beetles (Anophthalmns) respond to the light of a candle (Marchal, 1910), and after complete blinding some insects, such as cockroaches, will settle preferentially in the dark,^ a reaction which may persist even after decapitation,^ while others are attracted to light.* It is to be noted that the dermal response to light need not be of the same type as the ocular response ; the two may, indeed, be mutually exclusive. Thus it will be remembered ' that the flat-worm, Planaria lugubris, is positively photokinetic so far as the dermal response is concerned while it orientates itself by a negative phototaxis through the eyes (Viaud and Medioni, 1949). Again, the receptors in the skin and the eyes may show different sensitivities. Thus Viaud (1948) found that in some organisms the maximum response of the dermal mechanism was elicited by wave-lengths at the short end of the visible spectrum (the water-flea, Daphnia ; the rotifer, Branchionus) while the eyes responded preferentially to wave-lengths about the middle of the spectrum. A com- bination of the two mechanisms in the same organism may thvis involve two maxima in the response (as in the fruit-fly, Drosophila). Daphnia ^ p. 115. 2 p_ 537 3 For reviews, see Willem (1891), Dubois (1892), Nagel (1896). Viaud ( 1948) whose views have already been discussed on p. 31. 4 i.'A/^eito— Graber (1883) ; PeW;j7aneta— Brecher ( 1929). ^ The larvsG of the meal-worm, Tenebrio — Tucoleseo (1933). M erpillars— Lammert (1925), Suffert (1932), Oehmig (1939). ' p. HtJ, See especially THE GENESIS OF THE EYE 115 Specialization, however, occurred at a very early stage, for some degree of a localization of the sensitivity to light is seen even among Protozoa. The most elementary expression of this advance is the accentuation of photosensitivity in one part of the cell, and since the early response to the stimulation of light was motorial, this occurred particularly in the anterior part of the organism or in close association with the organs of locomotion, as is seen in the eye-spots of Flagellates and Ciliates ; an appreciation of directional activity was thereby gained. When unicellular organisms developed into multicellular, however, the subdivision into cells gave the opportunity for more intense specialization, and out of the generalized dermal sensitivity, specific integumentary liglitsensitive cells were evolved ; these again tended to accumulate in localities where the recejition of stimuli was of most biological value — towards the head-end of the animal, as in annelid worms, or in association with the motile organs such as the tentacles of Coslenterates, or the siphon or mantle of Molluscs. Such a single cell, however, although able to appreciate the presence of light, is unable to form images ; for this purpose a number of photosensitive cells must be aggregated together to form an " organ". The most primitive organ of this type is composed of a simple colony of independent cells without functional relationship — the simple eye or ocellus — and eventually such a grouj^ing of cells became structurally and functionally related in the compound eye ; in either case the receptor cells were usually provided with a focusing arrangement to concentrate the light and a j^igment mantle to absorb any excess. In this way eyes are found in some polychsete worms and higher Inverte- brates which from the anatomical point of view can form the basis of vision of varying degrees of sensitivity and resolution. Throughout Invertebrates there is therefore a wide range of photoreceptor mechanisms ; they have, however, one thing in common — that in contradistinction to the " cerebral eye " of Vertebrates, which is essentially of one general type and is developed from the neural ectoderm, with few exceptions (e.g., Rotifera) they are all derived from the surface epithelium. It is to be remembered, however, that in some Invertebrates, in addition to the integument and its derivatives, portions of the central nervous system appear to be light-sensitive. This api^lies, for examj)le, to the sixth abdominal ganglion of the crayfish (Prosser, 1934) ; in the eyeless white cave crayfish, Cambarus ayersii. Wells (1952) found that stimulation of the cerebral ganglion by light results in an increased kinesis without the suggestion of a visual sense. This is analogous to the light -sensitivity of portions of the central nervous system, particularly of the ependymal cells, of some Vertebrates,^ and the gonadotrophic action of light on the hypothalamus of some birds such as the duck ^ (Benoit et al., 1952). Drosoph ila Rotifer p. 537. p. 559. 116 THE EYE IN EVOLUTION It is interesting that to a certain extent " photoreceptors " may be seen in the vegetable world with an appropriate structural differentiation. Some plant cells, for example, may be raised up and rendered more convex with a lens-like thickening of the cuticle so that they may collect and concentrate the light more easily on the chloroplasts underneath (Haberlandt, 1901) (Fig. 76). This forms a receptor organ comparable to that seen in many animals — a veritable eye. The range of photoreceptive mechanisms seen in Invertebrates is wide, and far exceeds in its complexity the degree of vision which has hitherto been functionally demonstrated in many species, but at the same time it is probably legitimate to correlate function with structure to some extent. In the Protozoa we presumably have merely a common irritability, from which we may deduce a sentiency without specific characteristics.^ With the appearance of multicellular animals specialization became possible so that some of the cells in the outer layer could acquire a specific response to various types of stimuli. When the receptors thus be- FiG. 76.— Protonema of Schlstosteua , , n i-rv. j ■ i ^ -i otiMusDACEA. camc structurally dirierentiated, it The feeble light available in the may be assumed that a correspond- habitat of the plant is concentrated by j^g differentiation in function be- the lens-shaped cells upon the chloro- " -i i -n plasts underneath. came possible. Four mam groups or modalities appeared — mechano-, chemo-, thermo- and radio -receptors ; of these the first was probably the most fundamental, but the last, although originally the least im- portant, in subsequent evolution has far transcended the others by virtue of its greater potentialities in being able to project itself, as it were, into the distance. The development of " distance " receptors and of the projicient senses is late. Indeed, it has been suggested that radio -receptors only acquired their attributes as distance-receptors secondarily and that appreciation of light and darkness originated in a ^ahotoreceptor sensitive to a photochemical change in a substance with which it was in contact. The sea anemone appears to possess I)hotoreceptors of this simple kind (von Uexkiill, 1909), and a similar faculty is present in the skin of the ammocoete larva of the lamprey (Parker, 1903-5) and in numerous Amphibians (Nagel, 1896). This tendency, of course, is not confined to vision, l^he touch-spots of the skin have been projected in certain Carnivora to the tips of vibrissae so that exploration of the immediate environment is rendered more easy,^ while the glorified mechano -receptoi's of the organs of Corti respond to vibrations from a wide ;: ; ea in space of an amplitude considerably less than the diaineter of the hydrog > atom (von Bekesy and Rosenblith, 1951). Similarly, the heat-spots 1 p. 36. - For a general study, see Fitzgerald (1940). Ammocoete larva of lamprey THE GENESIS OF THE EYE 117 of the skin become prtijected in the temperature receptors seen in vipers in which a facial pit -like " eye " has developed for the reception of infra-red radiation (Bullock et al., 1952-56).^ The eye, of course, has transcended all other organs in this respect, projecting itself to astronomical distances and responding to a few qvianta of luminous energy. Originally it is probable that within the main groups, or modalities, appreciation was relatively undifferentiated ^ ; for example, a usual accompaniment of the radio -receptors is an absorbing pigment, and it is possible that the early pigmented cell responded to thermal energy as well as to luminous radiation. Subsequent evolution, both in the receptors and in their cerebral connections, determined not only an increase in the number of modalities (touch, temperature, smell, sight, hearing) but eventually led to the differentiation of various individual receptors within the same modality, thus allowing the emergence of qualities within a modality, such as colour within the modality of sight. PIGMENTS PIGMENT is a common feature of photoreceptors of all tyjDcs ; indeed, Bernard (1S97) suggested that light-sensitive cells first arose as modifications of the epidermis induced by crowding of pigment granules in situations which were most frequently and brilliantly illuminated. The physical energy of light can be converted into physiological activity only in so far as it is absorbed, and the primary function of the deposition of pigment in the neighbourhood of light-sensitive areas is to serve as an absorbing agent ; a further development is the initiation of a specific photochemical reaction. In its simplest form, pigment may aid the general dermal sensitivity to light, a function well illustrated in Echinoderms. Thus the entire surface of the sea-cucumber, Holothuria, is photosensitive and is coloured by two greenish-yellow pigments ; the reaction of the animal varies with the amount of pigment present, for young and lightly pigmented individuals are poorly light-sensitive while heavily pig- mented adults are markedly so (Crozier, 1914-15). Again, the sea- urchin, Centrostephanus Joricjisinnus. shows a high light-sensitivity in the violet spicules around the anal orifice whence a purple pigment can be extracted (von Uexkiill. 1900) — an early example, incidentally, of the frequent aggregation of sensory organs around the body orifices. When, however, specific light-sensitive organs are developed, pigment is concentrated in tlieir vicinity — melanin as an absorbent and visual pigments as sensitizers. All these pigments are synthesized by special cells called ciiromatoblasts {xpojyt-y.. colour ; ^Xxaros, a sprout). 1 See further, p. 600 « p. 109. Holothuria Cetitrostephanus ^- 118 THE EYE IN EVOLUTION MELANIN MELANIN (jLte'Aas-, black) is the common dark brown pigment ; it is elaborated locally by the organism from a colourless precursor found in the nucleus of special cells (melanoblasts). Very inert chemically, it acts merely as an absorbing agent. Melanin is a close relative of adrenalin and was originally thought to be derived from the blood (Scherl, 1893 ; Ehrmann, 1896 ; Augstein, 1912), but at an early date it was shown to have nothing in common with the derivatives of haemoglobin. A cellular origin therefore being necessitated, Kromayer (1893) and Hertwig (1904) suggested that it was derived from the nucleus, and Meirowsky (1906) narrowed this down to the nucleolus owing to the demonstration of large quantities of pyronin (a nuclear constituent) in melanotic cells, a view which appeared to be substantiated by the finding of this material in melanotic tumours by Rossle (1904). A further advance was made by von Szily (1911) who showed that the pigment was formed from a colourless precursor by the action of a ferment. Masson (1913) established that the action was oxidative in nature, and Bloch (1917) cleared up the matter by demonstrating that the cells of pigmented regions contain a specific intracellular oxidase. Bloch then isolated from the embryo of the broad bean 3-4-dihydroxyphenylalanine, a substance which he conveniently called "dopa", and showed that it was readily changed by this oxidase to melanin. When this svibstance is added to the epidermal cells of skin in frozen forn^alin-fixed sections, granules of melanin are formed (the " dopa reaction "). A large nvunber of the groupings in the protein molecule form coloured products on oxidation (tyrosine, jDhenylalanine, tryptophane, etc.), and it seems obvious that melanin, like adrenalin, is formed as an end- product from one of these chromatogen groups. Bloch concluded that the colourless " mother substance " (or melanogen) is almost certainly either identical with or related to " dopa " ; this colourless substance is brovight by the blood-stream to the cell ; here it meets the " dopa-oxidase " and thus is turned into the coloured pigment melanin. THE VISUAL PIGMENTS Photochemical and sensitizing reactions in both plants and animals, both phototactic and visual, depend almost universally upon one distinctive and compact group of substances, the carotenoids — a striking indication of the close evolutionary relationship between phototropism and vision. These form a number of pigments varying in colour from red to yellow, fat-soluble and highly unsaturated, occurring alone or as the prosthetic groups of proteins ; all of them seem to be related to the chromophore moiety of visual purple and are identifiable by their absorption spectra, the maxima of which usually lie somewhere towards the blue side of the mid-region of the visible band. As we have seen in a previous chapter ^ they also have a wide integumentary distribution among many species where they may play a dnr atic part in the coloration of the animal. Their high concentrati; 1 in the sex-glands (the interstitial cells of the gonads, the 1 p. 87. PHOTOPIGMENTS 119 adrenal and renal cortex) is a further point of association between the action of hght and sexual activities ^ (Goodwin, 1950). In the vegetable kingdom the predominant carotenoids are j3-CAR0TENE, C40H56, and XANTHOPHYLL, C4oH54(OH)2 — jellow pig- ments absorbing preferentially blue light with absorption spectra quite diflferent from that of chlorophyll. The latter and its relatives are active in the photosynthesis of plant metabolism and have no effect upon phototropic responses ; the former and its derivatives are concerned in photoreception in systems mediating orientation to light, they are pecuharly susceptible to the blue end of the spectrum, and are found only in the photosensitive parts of plants, such as the oat coleoptile 10 z 0 0 8 06 2 \~- 04- X LU 02 0 —t Y — A ^»s 400 500 Way/zlenqt'h ~mu. 100 80 60 40 20 0 c Fig. 77. — Spectral Sensitivity of the Phototropic Bending of Plants, AND THE Absorption Spectra of the Associated Carotenoids. Absorption spectrum (extinction) of the total carotenoids of the etiolated oat coleoptile, Avena ; continuous line (after Wald). Relative spectral sensi- tivity of the oat shoot ; broken line (after Johnston). (Voerkel, 1933 ; Castle, 1935 ; Biinning, 1937 ; Wald, 1943). Wald (1945-46) brought out this relationship dramatically by a study of the absorption characteristics of the phototropic response ; he found that the active spectrum of the phototropic bending of the seedling of the oat, Avena, was maximal in a blue light of 440 m/x and corresponded very closely with the absorption spectrum of the carotenoids extracted from the coleoptile (Fig. 77). The phototactic movements of animals, so far as they have been investigated, are also determined by carotenoids but in these the single maxima of absorption are disjDlaced to wave-lengths considerably longer than those associated with the phototropic bending of plants (473 to 534 niju) (Mast, 1917 ; Laurens and Hooker, 1920 ; Luntz, 1931). The pigment responsi])le for phototactic activity in a number of the green 1 p. 16, 120 THE EYE IN EVOLUTION Flagellates {Eucjlena, etc.) has been identified as astaxanthin (di- hydroxy di-keto /3-carotene, C40H52O4) (Tischer, 1936-38; Kiihn et al., 1939) ; this pigment is found only in animal tissues, is produced by the modification of ingested plant carotenoids, and, depending on its chemical nature, may range in colour from blue to red with varying characteristics of absorption. The pigments associated with the photoreceptors of the lower Invertebrates have not been fully investi- gated, but the available evidence indicates that the phototropic responses of the polyps of Coelenterates ^ and the siphons of clams, ^ as well as the phototactic activity of worms, ^ are also mediated by pigments of the astaxanthin type (Fig. 78). On the other hand, when image -forming eyes are reached in Z o ^ X UJ 10 08 0 6 04- 0-2 0 ■^^^'si^ — 100 80 60 40 20 0 400 500 600 Wave/enohh -mu Fig. 78. — Spectral Sensitivity for Photo-orientation of the Green Flagellate. Absorption spectrum (extinction) for astaxanthin dissolved in hexane ; continuous line (after Wald). Relative spectral sensitivity of Euglena viridis ; broken line (after Mast). Molluscs and Arthropods, the power has been gained to degrade vegetable carotenoids into the vitamin A system. Thus among Molluscs, the retina of the squid, Lolicjo pealii, has been found to have considerable quantities of retinene^ and vitamin A^ which, combined with a specific protein, produces a pigment with absorptive charac- teristics resembling those of rhodopsin (Wald, 1941 ; Bliss, 1943-48 ; St. George and Wald, 1949 ; Hubbard and St. George, 1956). It would appear that in the squid this reddish photopigment is a non- photosensitive type of rhodopsin, for which reason it was distinguished as cephdiopsin b}^ its discoverer (Bliss, 1948). ^ Hydioids of Sertularia and Eudendriuw , maximum absorption 474 m/u, Loeb and Wasteiii -s (1915). ^ Mya. iximum absorption 490 ni/it, PJiolas, maximum absorption 555 m/x, Hecht (191; * The eji i irm, Lumhricus lerrestris, and the larva? of the marine worm, Arenicola, maximum abs. ion 483 m/i. Mast (1917). PHOTOPIGMENTS 121 Vitamin A^ has also been isolated in quantity from the eyes of a number of marine Crustaceans,^ and the occurrence of this photo- chemical system in the eyes of the king-crab, Limidus, and of Insects has been corroborated by studies of their spectral sensitivity (Graham and Hartline, 1935 ; Jahn, 1946 ; Granit, 1947 ; Jahn and Wulff, 1948 ; and others) and also by behavioural experiments (Weiss, 1943). It is evident that more than one ty^e of pigment exists belonging to the vitamin A^ family ; thus among the shrimp-like euphausiid Crustaceans, Kampa (1955) isolated a pigment [Euj^hausiojisin) ^ with a maximum absorption of 462 m/x, and in the deep-sea pra-wn, Pandalus, an isomer was detected by Lambertsen and Braekkan (1955), It is true that in some of these organisms astaxanthin may also be found ^ MO Wavelength -ny^ Fig. 79. — Spectra of the Rhodopsin and Porphyropsin' Systems Direct spectra of crude preparations from the retinae of the marine scup (broken hnes) and the freshwater cahco bass (continuous lines). Rhodopsin and porphyropsin are dissolved in 1 per cent, aqueous digitonin solution, the retinenes and vitamins A in chloroform. All maxima have been brought to the same height to facilitate comparison (Wald). but this pigment appears to take no part in the visual process and is also distributed throughout the integument (Wald, 1941-46). Among Vertebrates the primitive Cyclostomes still retain the vitamin A^ system (visual jDurple) (Steven, 1955) associated with their retinal rods, as also does the majority of marine fishes ^ so far examined ; on the other hand, most fresh-water fishes ^ possess a different svstem based on vitamin Ao and retinenco. In Amphibians and hioher 1 Crabs, lobsters and others, Wald (194.5-46), Fisher et al. (1952-5.5). ^ Possibly related to or identical with the pigment absorbing maximally at 467 m/x described by Dartnall (1952) in the tench. ^ As in the fresh-water crayfi.sh, Caniharus virilis ; the shrimp, Aristeomorpha, Grangaud and INIassonet (1950). ^ Exceptions are found, for example, among the wrasse fishes {Labrus bergylta and Tautoga onitis), the eves of which have a pigment based on the vitamin Aj svstem (Bayliss et al., 1936 ; Dartnall, 1955). * An exception is the fresh-water bleak, Alburr^us lucidiis, which has, in addition to two pigments based on vitamin A,, another probably ba.sed on Aj (Dartnall, 1955). It is to be remembered, however, that only a few species have hitherto been examined so that further iii\estigation may weaken this generalization. 122 THE EYE IN EVOLUTION forms in the vertebrate phylum the vitamin A^ system is again encountered. Wald (1939-56) considered that two specific pigments were concerned — rhodopsin (visual purple) with the vitamin A^ system and porphyropsin (visual violet) with the vitamin A 2 system (Fig. 79). Evidence is rapidly accumulating, however, that the matter is not so simple, for it would appear that each of these does not repre- sent a single specific pigment ; both vitamins Aj and A 2 can exist as a number of isomers some of which combine with suitable proteins to yield photosensitive pigments of distinctive absorptive properties, several of which have already been discovered. Rhodopsin should therefore be interpreted as a generic name for all visual pigments associated with the rods based on vitamin A^, while porphyropsin is best similarly interpreted as embracing several rod -pigments based on vitamin A 2 (see Dartnall, 1957). The photosensitive pigments so far claimed — although with little substantial evidence — to be present in vertebrate cones — iodopsin associated with the vitamin Aj system and cyanopsin associated with vitamin A 2 — are also related carotenoid-proteins (Wald, 1937-55 ; Bliss, 1946) ^ ; on the other hand, accessory needs in the visual system such as the yellow pigment of the human macula are said to be met by xanthophyll — the intact carotenoid which mediates photo- reception in plants. The multiplicity of pigments of these two general types associated with the visual system is becoming increasingly apparent, and odd varieties have been discovered in special circumstances, differing considerably from the main groups. As we have seen, fresh -water fish usually have a pigment of the porphyropsin family, salt-water fish of the rhodopsin family ; euryhaline and migratory fishes which adapt themselves to both fresh and salt water therefore present an interesting problem. Since their spectral absorption curve is intermediate between that of rhodopsin and porphyropsin, Wald (1941) concluded that their retinae contained a mixture of both ; but it has been shown by Munz (1956) that in one at least of these fishes (the mud-sucker, Qillichthys mirahilis) the retina contains a single homogeneous pigment characteristic of the retinene^ type with an absorption maximum intermediate between the two main groups (512m!JL). Again, the gecko (Gekko gekko) has an unusual spectral sensitivity curve, similar to the human scotopic curve but with its maximum displaced 20 to SOmji, towards the red end of the spectrum (Denton, 1956). Retinal extracts from the Australian gecko, Phyllurus milii, have shown the presence of an unusual pigment with an absorption maximum at 524m(ji, typical of the retinene^ system but intermediate between the rhodopsin of the rods and the iodopsin of the cones (Crescitelli, 1956). This is interesting in view of the theory that the rods of this nocturnal animal may be transmutations from the cones of ancestr i cUurnal lizards.^ Pigments of unknown composition and tinknown function which appear, ^ In tilt -es of primates three pigments have been detected: chlorolabe (a green- absorbing ]i nt), erythrolabe (red-absorbing), and cyanolabe (blue-absorbing). See Vol. IV, p. 4 2 p. 252. PHOTOPIGMENTS 123 however, to differ from the preceding, have been found in the eyes and also in the integument of Arthropods among which they appear to have a wide distribution. They have been most fully studied in the eyes and integument of Insects and were first cursorily examined by Chauvin (1938-41). Becker (1939-41), studying these pigments in the ommatidia of a number of insect sjaecies, gave them the generic term ommochromes and subdivided them into ommins and ommatins. In certain insects, such as the fruit-fly, Drosophila, for example, he described a purplish-red pigment (erythrommatin) and a yellowish-brown (phgeommatin). During pupal development the brown pigment appears first and the red later, their appearance being determined by hormones, and one or other or both of the pigments may be absent in certain stocks, the eyes appearing respectively brown, red or white, ^ At a later date, however, Goodwin and Srisukh (1950) and Goodwin (1950), working on locusts (the desert locust, Schistocerca gregaria, and the African migratory locust, Locusta migratoria), concluded that these pigments represented a redox complex, yellow when oxidized and wine-red when reduced. For this variable pigment, or group of very closely related pigments which are at the moment indistinguishable, they suggested the name insecto- BUBIN, in view of its widespread distribution among insects. Whatever its chemical nature, it is very resistant to chemical attack, bat has been isolated as a reddish-brown powder which quickly changes into a stable dark brown powder reminiscent of melanin, and shows characteristic absorption spectra differing according to the method of extraction, whether measured in the fresh extract or in tlie reduced or oxidized forni. Related pigments with similar absorption curves have been described in crustaceans (the shrimps, Leander and Crangon — Polonovski et al., 1948 ; the fresh-water Amphipod, Oammarus pulex — Michel and Anders, 1954). Such is the general evolutionary story of the photopigments ; it is a large subject which will be discussed more fully when we deal with the physiology of vision in a subsequent volume. In passing, however, it is interesting to note that many years ago Patten (1886) put forward the theory that photoreceptors were originally evolved, not as sentient organs, but as receptors of light-energy for metabolic purposes as occurs in plants. He called them heliophags. The theory, however, in its time raised a storm of criticism and never received credence ; the most cogent evidence against it is the completely different chemical nature of chlorophyll and the carotenoids and the contrast in their functions — metabolism on the one hand, and photoreception or integumentary coloration on the other. Augstein. Klin. Mbl. Augeuhcilk., 50 (1), Bernard. Quart. J. micr. Sci., 39, 343 1 (1912). (1897). Bayliss, Lythgoe and Tansley. Proc. roy. Bliss. J. gen. Fhysiol.,26,^Ql (l9iS) ; 29, Soc. B, 120, 95 (1936). 277 (1946). Beadle. Gene^/cs, 22, 587 (1937). J. biol. Chcm., 172, 165; 176, 563 Beadle and Ephrussi. Genetics, 21, 225 (1948). (1936). Bloch. Hoppe Seyl. Z. physiol. Chem., 9S, Becker. Biol. Zbl., 59, 597 (1939). 226 (1916-17). Naturwissenschaften, 29, 237 (1941). Bohn. Actions directrices de la lumiere, v. Bekesy and Kosenblith. Hb. e.vp. Paris (1940). Psychol. (Stevens), 1075 (1951). Braim and Faust. E.vperientia, 10, 504 Benoit, Assenmacher and Manuel. C. R. (1954). Acad. Sci. (Paris), 235, 1695 (1952). Brecher. Z. vergl. Physiol., 10, 497 (1929). 1 See Beadle and Ephrussi (1936), Beadle (1937), Ephrussi and Beadle (1937), Mainx (1938), Ephrussi (1942), Ephrussi and Herold (1944), Wald and Allen (1946), Villee (1947), Maas (1948), Okay (1948), Nolte (1954). 124 THE EYE IX EVOLUTION Bullock and Cowles. Science, 115, 541 (1952). Bullock and Diecke. J. Physiol., 134, 47 (1956). Bullock and Faulstick. Fed. Proc. 12, 22 (1953). Biinning. Plaixta (Bed.), 26, 148, 583, 719 (1937). Castle. Cold Spr. Harb. Symp. quant. Biol.,Z, 224 (1935). Chauvin. C. R. Acad. Sci. (Paris), 207, 1018 (1938). Ann. Soc.etUom. France. 110, 133(1941). Bui . Soc. zool. France. 69, 154 (1944). Crescitelli. J. gen. Physiol., 40, 217 (1956). Crozier. Amer. J. Physiol., 36, 8 (1914). Zool. Jb., Abt. Zool. Physiol., 35, 233 (1915). Cuenot. Arch. Biol. Paris. 11, 313 (1891). Dartnall. J. Physiol., 116, 257 (1952) ; 128, 131 (1955). The Visual Pigments, London (1957). Denton. J. gen. Physiol., 40, 201 (1956). Dubois. Ayin. Unir. Lyon, 2, 1 (1892). Ehrmann. Bibl. Med., 2 (6) (1896). Ephrussi. Cold. Spr. Harb. Sytnp. quant. Biol., 10, 40 (1942). Ephrussi and Beadle. Genetics, 22, 65 (1937). Ephrussi and Herold. Genetics, 29, 148 (1944). Fisher, Kon and Thompson. J. marine Biol. Ass. Soc, 31, 229 (1952) ; 33, 589 (1954) ; 34, 81 (1955). Fitzgerald. J. Physiol.. 98, 163 (1940). Folger. J. Morphol., 42, 359 (1926). Biol. Bull., 53, 405 (1927). Goodwin. Biochem. J., 47, 554 (1950). Biol. Rev., 2b, 391 (1950). Goodwin and Srisukh. Biochem. J., 45, 263 (1949) ; 47, 549 (1950). Graber. S. B. Akad. Wiss. Wien.. Abt. 1, 87, 201 (1883). Grundlinien zur Erforschung des Hellig- keits- und Farbensinnes der Tiere, Leipzig (1884). Graham and Hartline. J. gen. Physiol., 18, 917 (1935). Grangaud and Massonet. C. R. Acad. Sci. (Paris), 230, 1319 (1950). Granit. Sensory Mechanisms of the Retina, Oxford (1947). Haberlandt. Ber. dtsch. botan. Ges., 569 (1901). Hecht. J. gen. Physiol., 1, 545, 657, 667 (1919) ; 2, 229, 337 (1920) ; 3, 1, 285, 375 (1921) ; 6, 731 (1924) ; 11, 657 (1928) Physiol. Rev., 17, 239 (1937). Hertwig. Fe.stschr. f. Haeckel ( 1 904). Hubbard aii! St. George. Fed. Proc, 15, 277 (HC Jahn. J. y. •; ^«/ow. .Soc, 54, 1 (1946). Jahn and \\ .J. X.Y. entom. Soc, 56, 109 (194- Kampa. Nature (Lond.). 175. 996 (1955). Knoop. Z. Beitr., 1, 219 (1954). Kromaver. Arch. mikr. Anat., 42, 1 (1893). Kuhn. Stene and Sorensen. Ber. dtsch. chem. Ges., 72, 1688 (1939). Lambert sen and Braekkan. Nature (Lond.), 176, 553 (1955). Lammert. Z.vergl. Physiol. ,2, 225 (1925). Laurens and Hooker. J. exp. Zool.. 30, 345 (1920). Loeb and Wastenevs. J . exp. Zool., 19, 23 (1915). Luntz. Z. vergl. Physiol., 14, 68 (1931). Maas. Genetics, 33, 177 (1948). Mainx. Z. indukt. Abstamm. u. Vererb- Ze/ire, 75, 256 (1938). Marchal. Richet's Dictionnaire de Physiol., 9, 273 (1910). Masson. C. R. Soc. Biol. (Paris), 75, 210 (1913). Mast. J. exp. Zool. 22, 471 (1917). J. Morphol., 41, 347 (1926). Protoplasma, 8, 344 (1929) ; 14, 321 (1931). Physiol. Zool., 5, 1 (1932). ^leirowskv. Mschr. prakt. Derm., 42, 541 ; 43, 155 (1906). IMichel and Anders. Xaturwissenschafteri, 41, 72 (1954). Millott. Philos. Tra72s. B, 238, 187 (1954). Endeavour, 16, 19 (1957). Munz. J. gen. Physiol., 40, 233 (1956). Nagel. Der Lichtsinn augenloser Tiere, Jena (1896). Newth and Ross. J. exp. Biol., 32, 4 ( 1955). Nolte. J. Genet., 52, 111, 127 (1954). Oehmig. Z. vergl. Physiol., 27, 492 (1939). Okay. Comm. Fac. Sci., Univ. Ankara, 1, 178 (1948). Pantin. J. marine Biol. Ass. U.K., 13, 24 (1924). Brit. J. exp. Biol, 1, 519 (1924) ; 3, 275, 297 (1926). Parker. Amer. J. Physiol., 10, 28 (1903) ; 14, 413 (1905). Patten. Mitt. zool. Stat. Xeapel, 6 (1886). Polonovski, Busnel and Grundland. C. R. Acad. Sci. (Paris), 226, 2182 (1948). Prosser. J. cell. comp. Physiol., 4, 363 (1934). J. comp. Neurol., 59, 61 (1934). Rossle. Z. Krebforsch., 2, 291 (1904). St. George, Goldstone and Wald. Fed. Proc, 11, 153 (1952). ' St. George and Wald. Biol. Bull., 97, 248 (1949). Scherl. v. Graefes Arch. Ophthal., 39 (2), 130 (1893). Schone. Z. vergl. Physiol., 33, 63 (1951). Steven. .J. exp. Biol., 32, 22 (1955). V. Studnitz. Pfliigers Arch. ges. Physiol., 243, 181 (1940). Siiffert. Z. Morphol. Oekol. Tiere, 26, 147 (1932). INVERTEBRATE EYES 125 V. Szily. .-Irc/i. /mX-r. .4nar, 77, 87 (1911). J. gen. Physiol., 22, 391, 775 (1939); Thines and Kahling. Z. Biol., 109, 150 25, 235, 331 (1941-42) ; 38, 623 (1957). (1955). Tischer. Hoppe Seyl. Z. physiol. Chein., Ainer. J. Phy.siol., 133, 419 {IMl). 239, 257 (1936) ; 252, 225 (1938). Viia7nins and Hormones, 1, 195 (1943). Tucolesco. Bull. Biol. Fr. Belg., 67, 480 Harvey Lecture Series, i^l, 117(1945-46). (1933). i^ed. Proc, 12, 606 (1953). V. Uexkiill. Z. BtoZ., 34, 315 (1897) ; 40, .4/i/i. i?er. B^oc^em., 22, 497 (1953). 447 (1900). Modern Problems in Ophthalmology, 1 Umwelt u. Innenwelt der Tiere, Berlin (Suppl. Ophthalmologica, 47), 173 (1909). (1956). Viaud. Experientia, 4, 81 (1948). Wald and Allen. J. gen. Physiol., 30, 41 Le phototropisme animal, Paris (1948). (1946). Viaud and Medioni. C. R. Soc. Biol. Weiss. Entom. News (Phila.), 54, 152 (Paris), 143, 1221 (1949). (1943). Villee. Genetics.32, 211 (1941). Wells. .4«a^ i?ec.. 113, 613 (1952). Voerkel. Planta (Bed.), 21, 156 (1933). WUlem. Bull. Sci. Fr. Belg., 23, 329 Wald. Nature (Lond.), 140, 545 (1937). (1891). THE STRUCTURE OF INVERTEBRATE EYES We are now in a position to study the various types of photo- receptors found among Invertebrates. In unicelhdar organisms the diffuse sensitivity to hght evolves into the locahzed sensitivity of an " eye-spot " ; in multiceHular organisms the diffuse dermal sensitivity evolves into the specialization of certain epithelial cells as specific photoreceptors. EYE-SPOTS : STIGMATA The earliest stage in the evolution of an eye is seen in unicellular organisms in which a small area of the protoplasm is differentiated to become specially sensitive to light ; this development is seen in actively motile ciliate and flagellate Protozoa, and since in these organisms light serves not as a visual but as an orientating stimulus, the specialized area is always in close association ^viih the cilia or flagella. Among Ciliates such specialization is primitive ; thus without observable structural differentiation, the oral surface of Stentor coendeus is more photosensitive than the aboral so that, as the organism rotates while swimming, successive exjjosures of these two areas determine a negative klinotaxis. orientating it away from the light (Jennings, 1904 ; Mast, 1 906-1 1).^ In Flagellates, however, a degree of structural differentia- tion appears which is sufficient to dignify the organelle thus formed with the name of an eye-spot or stigma {ariyiJix, a spot) ; there is a light-sensitive area, a mass of pigment which serves to make the organelle a directional detector useful in phototaxis. and occasionally a refractile structure wliich serves to concentrate the light, thus acting as a lens.- The stigma of tlie common green protozoon of ponds, Eugle?ia » p. 49. - As occurs in the Alg;p, Cladophora and Gonium (Mast, 1916). Stentor 126 THE EYE IN EVOLUTION viridis, is of the simplest variety (Fig. 80) ; the entire structure is about 5/x in diameter (Franz, 1893). The base of the single flagellum shows a thickening just anterior to its bifid root in the cavity of the reservoir ; it would seem that this is the photoreceptive area and it is BLIND SlD£ S£EIN0 SiD^ Fig. 80. — The Eye-spot of Euglesa viridis. A side view of the anterior end of the flagellate. /. The flagellum with an enlargement, e/, which constitutes the photoreceptive area. The two roots of the flagellum are anchored in the large contractile vacuole {cv.). Opposite the sensitive area is a shield of pigment (e) (after Wager, 1900). flanked on one side by a shield of the red carotenoid pigment, astaxan- thin (Engelmann, 1882 ; Wager, 1900 ; Mast, 1911-38 ; Buder, 1917 ; Tischer, 1936-38 ; Kuhn et al., 1939). It is interesting that Ehrenberg (1838), who first described this flagellate, assumed that the pigmented area was light-sensitive and considered that it constituted the most primitive eye in nature and called it the eye-spot (" Augenfleck"). It seems more probable, however, that it serves as an absorbing agent, shielding the flagellar swelling from incident light on one side and allowing it to be exposed on the other, so that as the organism rotates in swimming, the alternating stimulation and shading of the stigma affect the beat of the flagellum and directional phototaxis is attained.^ The instability of such an eye-spot is intei'esting. The Pringsheims (1952) found that if Euglena gracilis were grown at temperatures below the optimuni the pig- ment was lost and an apoplastidic race was produced in which the stigma disappeared if the organism were kept in the dark ; once lost, the eye-spot did not reappear. In certain Dinoflagellates, organisms which form an important part of the plankton of lakes and the sea, the 1 p. 48. Fig. 81.— The Eye- spot OF PoUCHETIA. Showing 1 hf large pigmented /- ■•, P, and the lens, '■■ ifter Schiitt). INVERTEBRATE EYES 127 stigma may be more complex. In Pouchetia, for example, the pignient is arranged in the form of a cup-shaped mass the opening of which is covered by a refractile structure, while within the cup, between the primitive lens thus formed and the pigment, lies the light-sensitive protoplasm (Fig. 81) (Schiitt, 1896) ; occasionally in the marine forms this structure is of such a size that it has been called an ocellus, but it is acellular. In all these cases the organelle combines photo- sensitivity with directional detection in order to perform its phototactic function. Buder. Jb. wiss. Botan., 58, 105 (1917). Biol. Zbl., 34, 641 (1914). Ehrenberg. Die Infusionsthierchen als Z. vergl. Physiol., 5, 730 (1927). volk-. Organi.smen, Leipzig (1838). Biol. Rev., 13, 186 (1938). Engelmann. Pfliigers Arch. ges. Physiol., .^ <. i t i /^ ? m • ; io 2Q 387 (188'^r Mast and Johnson. Z. vergl. Physiol., IQ, Franz. Z. wiss. Zool, 56, 138 (1893). "^^ (1932). Jennings. Pub. Carnegie Inst. Washington, Pringsheim, E. G. and O. New Phyto- No. 16, 256 (1904). logist, 51, 65 (1952). Kuhn, Stene and Sorensen. Ber. dtsch. Schutt. Ergebn. Plank, e.vped. (1896). c/^em.Ge^., 72, 1688(1939). J ^ i v j i r, Mast. J. exp. Zool., 3, 359 (1906) ; 20, Tiseher. Hoppe beyl. Z. physiol. Chem., 6(1916) ^ ' ''". 239, 257 (1936) ; 252, 225 (1938). Light and the Behavior of Organisms, Wager. J. Linn. Soc. (Zool.) Lond., 27, N.Y. (1911). 463(1900). LIGHT-SENSITIVE CELLS Once multicellular organisms evolved, the obvious specialization occurred whereby certain cells acquired a special sensitivity to light ; as would be expected, they were ectodermal cells initially developed in the surface epithelium although on occasion they migrated below the surface layer. Such cells may be found alone or may occur in associa- tion with others to form an eye ; and in either case they may assume several forms usually with well-defined characteristics, including a specially sensitive receptor as well as an arrangement to conduct away the excitation. Frequently the cell is associated with pigment which serves as an absorbing agent, a fimction which becomes all the more important when the sentient cells sink below the surface, in which case the receptive pole is frequently surrounded by a pigment mantle (Fig. 82). While thus aiding the receptor mechanism, an absorbing pigment mantle is not essential and, indeed, is frequently absent. The light-sensitive cell usually assumes a specialized form which may be differentiated into two main types. In the first and more common type two poles are distinguished — a distal to receive the stimulus of light and a jjroximal to conduct away the excitation. In the fully developed bipolar cell, therefore, three regions are apparent : a receptor or end-organ, a cell body with the nucleus, and a proximal prolongation into a conducting fibre. The recejitive end-organ of the cell is often found to assume a complicated form ; sometimes it is provided with digitations, presum- ably in an attempt to increase the receptor surface (Fig. 87) ; more frequently it undergoes specific modifications which can be classed as belonging to two main types, cilia and rods, the second presumably a 128 THE EYE IN EVOLUTION Figs. 82 to 85. — Types of Bipolar Visual Cell. Fig. 82. Fig. 83. J. Fig. 84. Fig. 85. Fig. 82. — The visual cell of the edible snail, Helix pomatia, showing cilia (after Hesse). Fig. 83. — The visual cell of the grey slug, Llnuix maximus, showing elongated end with cilia (after Hesse). Fig. 84. — The visual cell of the marine worm, Phniaria forva, showing brush-like border (after Hesse). Fig. 85. — Rod-like visual cell of the Tabanid fly, Cliry.b-ops marmoratus (after Ciaccio). specialized derivative in many ectodermal several types of sensor Fig. 86. — Apolar Visual Cell. A light-sensitive cell in the earthworm, LiDtibvi- cus terre.stris, stained with silver nitrate. N, nu- cleus ; OX, optic nerve which breaks up into a network of neurofibrils, CN, throu;^: out the cyto- plasm ; ()(i, optic orga- nelle coverev a, denser network of urofibrils to form ti ■.'tinella (after W. N. li ). of the first. 1 cilia (Figs. 82 and 83) are found cells and form an important differentiation of y cells, and it may be, as Hesse (1902) surmised, that they represent the distal terminations of bmidles of the " neuro-fibrillse " which form the primitive conducting mechanism ^ ; a similar configuration is seen in cells with a striated or brush-like border (Fig. 84). rods (or rhabdites) appeared originally as simple but stouter cylindrical prolongations of protoplasm, clear and refractile in nature, which in subsequent evolution have undergone innumerable speciali- zations (Fig. 85) ; they are found in worms, Arthropods, and Molluscs, and they attain their highest differentiation in the rods and cones which form the imique receptor apparatus in the eyes of Vertebrates. The second type of recejDtor is seen among worms and Molluscs ; in it the cell is apolar in its general arrangement but contains a light- sensitive mechanism within the cell body (Fig. 80). This typically takes the form of a 1 p. 243. 2 See VVorley (1933-41). INVERTEBRATE EYES 129 peculiarly shaped ellipsoidal mass — the optic organelle (the " Binnen- korper " of Hesse ; the " Glaskorper " of Apathy, 1897) — distinctly marked off from the rest of the cytoj)lasm by its deeper staining, occupying the centre of the cell and crowding the nucleus to one side ; it is made up of a clear hyaline-like structure (a " lens ") surrounded by a dense neurofibrillar network (the retinella). Hess (1925) found experimentally that no matter from which direction light was directed onto the cell, the " lens " brought it to a focus on the sur- rounding network of the retinella, a circumstance which suggests that the hyaline mass focuses the light which induces a direct stimulation of the nerve-fibres, possibly by a photo-electrical rather than a photochemical effect. Depending on the arrangement of these cells singly or in com- munities to form an organ, invertebrate eyes may be classified morpho- logically as follows. I. The SIMPLE EYE or ocellus. 1. The unicellular eye. (a) epithelial, (6) subepithelial. 2. The multicellular eye. (a) the subepithelial eye, (6) the epithelial invaginated eye. (i) the flat eye, (ii) the cupulate eye, (iii) the vesicular eye. II. Intermediate forms. (a) The aggregate eye. (6) The composite ocellus. (c) The simple ommatidial eye. III. The compound eye. The Simple Eye A simple light-sensitive cell, an ectodermal cell differentiated from its neighbours in order to receive incident light and transmit a physio- logical imjjulse, ranks as a very primitive type of eye. With single cells, each of which is responsive merely to the presence of light, a light-sense may exist, but no definite image such as is necessary for the development of the visual sense can be formed. If, however, these cells multiply and group together in clumps l^o form an " organ ", some conception of an object may be realized and a primitive directional analysis may be made of visual space. Each single constituent cell, it S.O.— VOL. I. 130 THE EYE IN EVOLUTION is true, merely records the sensation of light, but the summation of all their individual sensations will give an elementary mosaic or pattern of light and shade with a consequent impression of the external world. So long as the component cells of the group retain their individuality and act independently of each other, they may be considered to form a " simple " eye. The simple eye or ocellus (dim. of oculus, eye) may therefore be defined as a single light-sensitive cell or group of such cells acting ivithout functional association. Leucosolenia THE UNICELLULAR EYE Single cells which are responsive to light (" cellules visuelles " of Apathy, 1897 ; " Photores " of Beer, 1901) were first adequatel}^ described by Richard Hesse (1896) as occurring in the epidermal layer of worms ; he called them " Sehzellen ", but since in many cases they appreciate the presence of light for the purposes of jDliototactic reactions and are probably not associated with a visual sense as the term is generally understood, we shall call them light-sensitive cells. Shortly thereafter they were found in a large number of animals, sometimes scattered about indiscriminately but usually aggregated in those regions where they are of most importance to the organism. Thus in clams they are confined to the siphon, in some shell-fish are arranged like a coronet around the edge of the mantle, and in annelid worms they are concentrated at the two extremities, particularly the anterior.^ Unicellular eyes may assume either of the two forms of light- sensitive cell we have already discussed — the bipolar form with a specialized sensory termination or the apolar form characterized by an intracellular organelle. SINGLE BIPOLAR LIGHT-SENSITIVE CELLS are usually provided with a ciliate or brush-like border and are associated with pigment, usually placed as a cap around the light-sensitive end of the cell. They are seen in the unicellular photoreceptors of the larvse of certain sponges {Leucosolenia, Minchin, 1896) and in Rotifers, but occur most typically among worms. Examples of this are the light-sensitive cells of Tristomum papillosum, a Trematode parasitic on marine fishes (Fig. 87), or in Polyophthalmus pictus, a sedentary Polychsete which abounds in the Bay of Naples (Hesse, 1899- 1908). eye is interesting that the most primitive "cerebral " ordates, seen in the neural tube of Amphioxus^ 190. p. 230. Fig. 87. — Unicellu- lar Eye of the Trematode Worm, Tristomum papil- losum. The cell is provi- ded with a crenated border and piginent mantle (after Hesse). THE SIMPLE EYE 131 is similarly a single photosensitive neural cell associated with a pigment mantle (Fig. 238). SINGLE APOLAR VISUAL CELLS are typified in the light-sensitive organs of the earthworm, Limibricus terrestris ; these have received closer study than those of any other species (R. Hesse, 1894—97 ; Beer, 1901 ; Kowalski, 1909 ; W. N. Hess, 1924-25) (Figs. 86 and 88). They are found in two sites — ^in the epithelium and in association with the nerves immediately underneath ; it is probable, as has been shown in the medicinal leech (Whitman, 1893), that the latter originated in and migrated from the epidermal layer. In appearance they are distinctive. The superficial cells are small and rounded, lying at the base of the epithelium and into each the sub- epithelial nerve-net sends a nerve- fibre which breaks up into a network of neurofibrils surrounding the ellip- soidal optic organelle ^ ; the sub- epithelial cells clumped around enlargements of the nerve plexus are similar in type and presumably in function. It is interesting that a dense layer of pigment lies under the epithelium apparently unassociated with the light-sensitive cells ; but as they traverse this layer and run into the epithelium, the nerves make pin- point openings in the dense pigmen- tary blanket so disposed that incident light will enter, dorso -anteriorly at the anterior end of the worm and dorso -posteriorly at the posterior end, and will thus strike the subepithelial cells directly as either extremity emerges from the burrow. The light-sensitive cells of leeches are also of a very similar type, each containing an identical optic organelle supplied with a nerve fibre from the dorsal ganglion (R. Hesse, 1897). They may occur as isolated cells just below the epithelium or may lie in association with other sensory cells. ^ Light- sensitive cells identical with those of the earthworm are also found in lamelli- branch molluscs ; thus in the clam, Mya arenaria, they are seen, plentifully supplied with nerves, lying jvist beneath the epithelial layer on the inner surface 1 p. 128. 2 p. 1.3.3. Fig. 88. — Single Light-sensitive Cells in the Earthworm, Lim- BRICVS TERllKSTRIS. The photoreceptor cells, L, lying in tlie basal region of the epidermis, E, and also in enlargements of the nerve in close relation to the eijidermis. The nerve is seen to spread out beneath the epithelium as a subepidermal nerve plexus, the fibres of which go to the photoreceptor cells. C, cuticle (after W. N. Hess). 4fipii^i4uiuiS$&^^l^ Lumbricus Mya arenaria 132 THE EYE IN EVOLUTION of the siphon ; again, each contains an optic organelle with a surrounding nerve-plexus (Light, 1930). It is interesting that somewhat similar cells, presumably sensitive to light, have been described in the epidermis of the tail of the ammocoete larva of the lamprey (Steven, 1951).^ Apathy. Mitt. zool. Stat. Neapel, 12, 495 Kowalski. La Cellule, 25, 291 (1909). (1897). Light. J. Morph. Physiol., 49, 1 (1930). Beer. Wien. klin. Wschr., \^, 255, 29,5, Minchin. Proc. roj/. 5'oc. J5, 60, 42 (1896). 314(1901). Steven. Quart. J. micr. Sci., 92, 233 Hess, W. N. Biol. Bull., 38, 291 (1919). (1951). J. Mor/j/i., 39, 515(1924) ; 41,63(1925). Whitman. Zool. Jb., Abt. Anat., 6, 616 Hesse, R. Z. m«s. Zoo/., 58, 394 (1894) ; (1893). 81, 393 (1896) ; 62, 671 (1897) ; 63, Worley. Proc. nat. Acad. Sci., 19, 323 361(1898); 65,446(1899); 72,565 (1933). (1902). J. exp. Zool., 69, 105 (1934). Die Sehen der niederen Tiere, Jena J . cell. comp. Physiol., b,5Z {l^^'i) ; 18, (1908). 187 (1941). THE MULTICELLULAR SIMPLE EYE While the most primitive example of the simple eye is represented by a single light-sensitive cell, the next obvious development is the association of a group of epithelial cells each reinforcing the effective- ness of the others. For this purpose several evolutionary lines have been followed so that eventually the end-organ appears to reach a degree of complexity greater than the analysing capacity of the nervous organization. Efficiency is enhanced not only by the progressive development of the capacity to form detailed images as the number of sensory cells increases, but also of the ability thereby obtained to localize the stimulus in space and analyse the visual field (a directional eye). The association of pigment forming an absorbent screen within or around the sensory cells is a constant feature, while the efficiency of the organ is further increased by the development of a focusing apparatus. To this end a wide variety of optical mechanisms is exploited varying from a pin-hole to a lens-system of progressive elaboration until, in Cephalopods. a dioptric mechanism comparable to that of Vertebrates is reached. The inner ends of the sensory cells are prolonged to form elongated processes or nerve fibres which leave the deep surface of the ocellus to join a subepithelial plexus or a ganglion. The sensory cells usually remain in association with the surface layer but occasionally migrate inwards to the subepithelial tissues ; and since the latter type of ocellus undergoes less evolutionary develop- ment than the former, we will discuss it first. The Subepithelial Eye The fnigration of a number of light-sensitive cells from the surface with th( ■ aggregation in the subepithelial tissues to form a sub- epithelial > always results in an organ of a very elementary type. 1 p. 263. THE SIMPLE EYE 133 These cells may belong to either of the two main types we have just discussed. In the first place, we have already seen in the case of the earthworm that an aggregation of apolar cells with a central organelle in the cell-body may migrate from the surface epithelium to form a subepithelial mass in association with the nerve fibres (Fig. 88). Subepithelial eyes formed by the clumping together of a multitude of visual cells of this tjrpe within a dense pigmentary mantle are found in certain leeches. Figs. 89 and 90. — The Sensory Organs of the Medicinal Leech, HlRCDO Medici.\alis. Fig. 89. — The sensory organ of the inter- mediate'segments consists of a collection of undifferentiated sensory cells, S, among which are seen the large light- sensitive cells, V (4 in the figure), with the kidney-shaped hyaline optic organelle (after Biitschli). jg^trasOTiamjxr FiG. 90. — Each " eye "' situated in the anterior segments con- sists of a cluster of apolar cells provided with optic organelles, the whole being enclosed in a pigment mantle through which the nerve fibres travel, and Ij'ing beneath the surface epithelium (schematic after Hesse). The ocelli of the medicinal leech, Hirudo medi'^inalis, are of unusual interest since they show all stages of evolution from a unicellular to a multicellular eye. As we have noted, ^ typical apolar light-sensitive cells may occur lying singly, deep in the epithelium. On the dor.sal surface of the intermediate segments of the animal there are paired clusters of undifferentiated sensory cells derived from the epithelium, each cluster forming a segmental sensory organ the function of which seems to be essentially tactile ; among these cells there are several typical light-sensitive cells so that the colony presumably has a dual function (Fig. 89). On the anterior five segments these clusters of cells are purely visual and are clumped together in a cylindrical mass at right angles to the surface enclosed in a dense pigmentary mantle, forming subepithelial eyes (Fig. 90) 1 p. 131. Hirudo 134 THE EYE IN EVOLUTION HoBmadipsa (Whitman, 1889-93 ; Maier, 1892 ; Hesse, 1897-1902 ; Biitschli, 1921). In the land-leech, Hoemadipsa, the ordinary segmented papillfe more closely resemble eyes since the visual cells are associated with j^igment (Bhatia, 1956). In the second place, bipolar cells with a cihate or brush-like receptor and a proximal nerve fibre may similarly migrate into the subepithelial tissues, aggregating into a cluster in association with a mantle of pigment cells. These are seen typically in the leaf-like turbellarian and the ribbon-like nemertine worms (Figs. 91 to 93). In these, the eye consists merely of one or a number of elongated visual cells with a distal ciliated border, the fibrillar terminations of which run proximally to form an optic nerve ; the organ lies under the Figs. 91 to 93. — Subepithelial Eyes (after Hesse). Fig. 91. — The eye of the turbellarian worm, Planaria torva, consisting of two light cells with cilia (c), nucleus (71) and pigment mantle (p), the whole Ij'ing underneath the epithelium (e). r]~o] * I o|V|^"je|fr e HZ ™aaa, Fig. '.2. — The eye of the turbellarian '>)rm, Planaria gonocephala. Fig. 93. — The eye of the nemertine worm, Drepanophorus. THE SIJVIPLE EYE 135 epithelium and the elongated visual cells curve away from the surface to crowd into a cellular cup of densely pigmented cells. Such an organ in addition to being light-sensitive can appreciate the direction of incident light, and forms a primitive type of directional eye. A still more complicated organ of this type is seen in the paired eyes of Chaetognaths, such as the marine arrow-worm, Spadella (Hesse, 1902), and in the median eyes of certain Crustaceans.^ It is of interest that in this subepithehal type of eye the sensory pole of the cell is usually directed away from the incident light which has to traverse the cell -body in order to reach it ; technically, therefore, these are examples of an inverted retina.^ Chsetognath The Epithelial Invaginated Eye A much more common arrangement, however, is an association of a number of contiguous cells in the epithelial layer, which as evolution progresses eventually invaginate into the underlying tissues. In such a development the first stage is the specialization of a number of con- mii^ b Fig. 94. — Scheme of Development of the Simple Epithelial Eye of Invertebrates. (a) Single epithelial light-cell. (6) A group of light-cells forming a flat eye (Fig. 95). (c) The cupulate eye (Fig. 97). (d) The formation of a dark chamber (Fig. 100). (e) The vesicular eye (Fig. 110). (/) The eye of Cephalopods (Fig. 113). tiguous surface cells to form a plaque on the surface — the flat eye (Fig. 946) ; the second stage is evident when the epithelium becomes invaginated so that the sentient cells line a simple depression on the surface^ — the cupulate eye ; thus, while to some degree protected, their functional utility is increased by the crowding together of more units into the same space, and by an arrangement whereby they can orientate more accurately the incident light. A further improvement 1 p. 152. - p. 146. 136 THE EYE IN EVOLUTION is gained when the opening of the depression is narrowed so that a dark chamber with a pin-hole opening is formed. The last step in the differentiation of the simple eye is marked by the closure of the opening leading into the depression by a circular in-folding of the surrounding epithelium ; thus is formed the vesicular eye, the highest differentia- tion of which is reached in the eye of Cephalopods wherein the vesicle is associated with a secondary invagination of the ectodermal layer which, in addition to providing a protective covering, helps to constitute a dioptric mechanism. The scheme of the development of the simple eye from its primitive beginning as a single cell to this highly complex structure is seen in Fig. 94. The simiDlicity of these eyes is seen in their capacity for regeneration, a potentiality first demonstrated by Bonnet (1781). If the tentacle with the eye is removed from the edible snail or the grey slug, another regenerates, occasion- ally equipped with two eyes, a process which has been known to occur twenty times in succession (Galati-Mosella, 1915-17). ExiDerimenting similarly on the gastropod, Murex, Carriere (1889) found that the regenerating eye initially took the form of a simple depression, which gradually closed leaving only a pore-like opening and eventually developed into a closed vesicle. THE FLAT EYE This is the most primitive association of light-sensitive cells and usually consists of 5 or 6 epithelial cells lying upon the surface, differentiated by being a little larger than their unspecialized neigh- bours. Such an ocellus is seen in the aquatic worm, Stylaria lacustris Figs. 9.5 and 96 — Flat Eyes. Dendrocarhcm Fig. 95. — The ocellus of the aquatic amielid worm, Stylaria lacustris (after Hesse). Fig. 96. — The ocellus of the hydro- medusan, Lizzia, the epithelial sen- sory cells being capped by a lens-like thickening of the cuticle (Hertwig and Jourdan). (Fig. 95) (Hesse, 1908), in certain unsegmented planarian worms such as Dendrocoslum and some leeches, while in the larvae of some insects the eyes consist merely of a pair of visual cells and two overlying pigTi^ent cells (Hesse, 1908 ; Imms, 1935). Occasionally a simple cuti. ;lar refringent apparatus is added to collect the light as well as pignic ' t to absorb it ; thus in the hydromedusan, Lizzia, the eye, situa at the base of the tentacle, is composed of a number of sensory THE SIMPLE EYE 137 cells associated with j)igmented cells capped by a " lens " formed by a localized thickening of the cuticle (Fig. 96) (Hertwig, 1878 ; Jourdan. 1889). THE CUPULATE EYE The crpuLATE or cup-shaped eye {cupula, a cup) forms a distinct functional advance, for the invagination of the light-sensitive epithelium allows the development of a primitive directional sense (Patten, 1886). Its development may be seen in three stages. The first is a simple Figs. 97-100. — Typical Cupulate Eyes of the Simplest Type. Fig. 97. — The ocellus of the limpet, Patella. Ep, epithelium ; S, secretory sub- stance covering visual cells ; N, nerve (after Hesse). Fig. 98. — The ocelkis of the ear-shell, Haliotis. The cup-shaped depression is deep with a narrow neck and is filled with secretion formed by the epithelial cells (after Hesse). Fig. 99. — The visual organ of the larva of the house-fly, Musca. There is a small cavity in the cephalo-phar\Tigeal skeleton wherein lie light-sensitive cells, C, from which issues the optic nerve, N (after Bolwig). Fig. 100. — The ocellus of the mollusc. Nautilus, with its pin-hole opening (after Hesse). 138 THE EYE IN EVOLUTION ViGS. 101-3. — Representative Cupulate Eyes of a Moke Complex Type. Fig. 101. — The ocellus of the polychspte worm, Nereis. C, cuticle ; Ep, epithelmm ; N, nerve fibres ; P, pigment between the sensory cells ; R, nucleated sensory cells provided with cilia ; y, vitreous (after Hesse). Fig. 102.— The ocellus of the Cubo- medusan, C'harybdea. L, cellular lens ; V, " vitreous body " of the clear rhabdites of retinal cells ; P, pigmented zone of retinal cells ; R, retinal cells ; N, nerve tissue with ganglion cells, G (after Berger). ON CG Fig. 103. — The eye of Peripalns. Diagrammatic sagittal section of t}ie e\e ; partly depigmented to demons; i ate details of the visual cells. C lea ; CG, cerebral ganglion ; Ep, hypodermis ; L, lens ; OG, optic ganglio; ')N, optic nerve ; R, rods ; V, visual cells (after Dakin). THE SIMPLE EYE 139 depression or dimple in the epithelium, such as is seen typically among Molluscs ; some 30 such cup-shaped depressions, for example, each ^ mm. in diameter, skirt the border of the mantle of the bivalve, Lima, while similar structures are seen at the base of the tentacles of the common limpet. Patella (Fig. 97). The simple eyes of the larva of the house-fly, Musca, are of a similar type (Bolwig, 1946) (Fig. 99).^ In such cases the sensory epithelium may be composed of light-sensitive pig- mented cells interspersed with unpigmented secretory cells which secrete a protective material covering the epithelium. The second stage is marked by an overlapping of the surface epithelium so that the shallow pit becomes converted into a cavity with a tiny opening. Such a cup may be oval and deep and filled with secretion, as in the ear-shell, Haliotis (Fig. 98), but the tendency is seen in its most marked form in the rare pearly mollusc. Xaufilus. which lives in a beautiful spiral shell in the seas of the Far East (Fig. 100). In this cephalopod, situated just behind the tentacles, a pin-hole opening 2 mm. in diameter leads into a large ocular cavity lined by light-sensitive cells bathed by sea-water, the eye thus constituting a veritable dark chamber (Merton, 1905). In a third and final development the cavity is closed by the growth of the cuticle associated with hypodermal cells over the opening. Although a closed vesicle is thus formed, it is made up of the non- cellular cuticle which extends uninterruptedly over the cupula of the invaginated layer of cells, while the secretory mass elaborated by the sensory cells becomes enclosed to form a vitreous body (the marine polychgete worm. Nereis— Hesse, 1897-1908) (Fig. 101). Once this stage has been reached, further advances can be made in the optical arrangements of such an eye. The simplest is the more or less elaborate thickening of the cuticular layer of the epithelium to form a refringent apparatus. In its most primitive form such an eye consists merely of a group of visual cells arranged in a hollow beneath a lens formed from the cuticle as is seen, for example, in the medusoid, Sarsia, or the louse, Pediculus, or other insects (Fig. 106). A somewhat similar morphology is seen in the eye of the Onychophore. Perijmtus,^ but in it the large lens is formed from the hypodermal cells and takes the place of the vitreous (Fig. 103) (Cuenot, 1949). Usually, however. h\^odermal cells continuous, on the one hand, with the surface ectoderm and, on the other, with the sensory cells of the cupula, edge their way underneath the cuticle where they may form a clear, refractile mass underneath the cuticular lens constituting a primitive lens or vitreous (as in the ocelli of many insects and in some spiders. Figs. 104 and 105) (Biitschli, 1921; Wigglesworth, 1941; and others). Alternatively, as in the C'ubomedusan, Charybdea, the distal ends of the retinal cells (rhabdites) develop greatly to form a clear 1 p. 224. 2 p. 204. ^^^^a^miD Larva of Musca Nautilus Nereis Sarsia Pediculus Peripatus Figs. 104—9. — Cupulate Eyes of Arthropods. Fig. 104. — The frontal stemma of the imago of the blow-fly, Calliphora (after Lowne). Fig. 10.5. — Sagittal section of the median anterior ocellus of the jumping spider, Salticus (after Biit- schli). DIS Fig. 106.— The frontal oceUus of the hover-fly, Helophilus. DIS, cells with long sensory ends lying distant from the lens ; Pr, cells with short sensory ends lying proxi- mally to the lens (after Hesse). Fig. 107. — The anterior median ocellus of the house spider, Tegenaria domes- tica. It is to be noted that the optic nerve fibres, ON, issue from the lateral aspect of the visual cells, R (compare p. 159). Fig. 108.— The dorsal ocellus of the insect, Aphrophora spumaria (after Fig. 109. — The lateral ocellus of the scorpion (after Lankester and Link). Bourne). In Figs. ! ()H-9 the eye is in every sense simple although there is some association of the visual > .• lis around rhabdon>«s. Cut, cuticle ; Ep, hypodermal epithelium ; L, cuticular lens ; N, ON, optic nerve fibres ; P, p nent cells ; PS, preretinal space ; R, retinal (visual) cells ; Rd, rods or rhabdites ; i rhabdomes ; V, hypodermal cells forming vitreous. THE SIMPLE EYE 141 "vitreous" mass (Fig. 102) (Berger, 1898; Berger and Conant, 1898-99). The lens may thus be aceUular and cuticular, or cellular ; the vitreous cellular or gelatinous, formed either a3 a secretion of the retinal cells or by their degeneration and coalescence. An interesting modification is seen in the stemmata or simple eyes of the larval and pupal forms of some insects such as sawflies (Ten- thredinidse) and many beetles (Coleoptera) as well as in the ocelli of most adult insects, in the lateral eyes of the scorpion (Figs. 108-9), and the median eyes of the king-crab, Limulus (Fig. 142) ; in these the visual cells are arranged in loose groups of two or three around a rod- like structure secreted by the visual cells — the rhabdome (/ia^Sajyiia, a rod). Such an arrangement does not alter the essential simplicity of the eye. It has been suggested that some accommodative adjustment of a static type may be provided in these eyes by the existence of differences in the distance between the sensory cells and the lens (some flies, as Helojjhilus) (Fig. 106) (Hesse, 1908). THE VESICULAR ETE The final stage in the evolution of the simple eye is the closure of the invaginated epithelium to form an enclosed vesicle divorced entirely from the surface ectoderm and usually separated from it by mesen- chyme. In its simplest form such an eye is merely a spherical vesicle lined with ectodermal cells ; the cells of the proximal (deep) part of Helophilus Fig. 110. — The Vesicular Eye. The ocellus of the edible snail. Ep, epithelium ; vs, visual cell ; pc, pigment cell ; n, nerve (after Hesse). 142 THE EYE IN EVOLUTION Buccinum Helix the vesicle are partly light-sensitive, partly secretory, the former being frequently associated with pigment and connected by nerve fibres with the oi^tic or cerebral ganglion ; the distal (superficial) elements are rela- tively undifferentiated, and a refractile mass of secreted material, homologous M'itli the vitreous of higher types, fills the cavity. Such a simple ocellus, lying in the subepithelial tissues over which the epithelium passes without interruption, is seen most particularly in Gastropods such as Murex which furnished the Tyrian purple,^ the common whelk, Buccinum, or the edible snail, Helix pomatia (Fig. 110). Its most elaborate form is seen in tlie spider- or scorpion-shell, Pterocera lamhls, a gastropod found on tropical reefs, wherein the vesicle, filled with a vitreous-like material, has a clear tlistal wall (a cornea), while the proximal part a i'iu. 111. — TiiK Ketina of Ptehoceua lambis. The retina contains four layers : (a) a layer of rods ; (b) a layer of pigment cells containing some rod nuclei ; (c) a cellular layer in which are distin- guishable most of the rod nuclei, bipolar cells, a few horizontal cells, ganglion cells and supporting cells with a reticulum resembling Midler's fibres in tlie vertebrate retina ; (d) a layer of optic ner\e fibres (J. H. Prince). of the vesicle is occupied by a retina consisting, according to Prince (1955), of 4 layers — (a) most distally, a layer of rod -like visvial cells, (6) a layer of pigment cells, (c) a cellular layer containing the nuclei of the rods, synaptic "bipolar", " horizontal " and ganglion cells, and {d) a layer of ojjtic nerve fibres, the axons of the ganglion cells which leave the eye in nvimerous optic nerve bundles (Figs. Ill and 189). With a receptor population ajaproaching 10,000 per scj. mm., the sensitivity of the eye is j^robably considerable although, in the absence of an efficient optical system, image -format ion must be verj^ deficient. In a further stage of complexity a lens is added to the vesicular eye so as to form a camera-like eye resembling that of vertebrates ; an accommodative mechanism and an extra-ocular musculature are provided. This is typically seen in two very different phyla : among the Polychsetes in the family of Alciopidae, and among the Cephalopods whic> have the most elaborate eyes in the invertebrate kingdom. ^ Set? Singer, The Earliest Chemical Industry, London, pp. 12-14 (1948). THE STIMPLE EYE 143 The remarkable eyes of the Alciopidse, a family of pelagic polychsetes {Alciopa, Vanadis, etc.), have received considerable study ^ (Fig. 112). In these worms the proximal part of the vesicle is occupied by a retina with direct receptors ; the main body of the vesicle contains a vitreous-like mass of two consistencies, separating the retina from the anteriorly situated lens. The posterior portion of the vitreous is jelly-like and is secreted by the intercalary cells of the retina ; the distal portion is derived from a glandular cell situated ventrally. There is an effective accommodative mechanism - and the eyes are moved by 3 extrinsic muscles. Nothing is known about the function of these elaborate eves. Fig. 112. — ^The Eye of the Polych.ete Worm, Va.\adi^. BV, blood vessels ; CT, connective tissue ; DV, distal vitreous ; G, ganglion cells ; GC, glandular cell secreting the distal vitreous ; L, lens ; ON, optic nerve ; NF, optic nerve fibres ; PR, proxiinal retina ; PV, proximal vitreous ; R, main retina showing the rods separated from the visual cell-bodies by a dense line of pigment (after Hesse). The eyes of the dibranchiate cephalopods (cuttlefish, squids, octojxis, etc.) have received a considerable amount of study (Figs. 113, 114).^ The two eyes are set on pedicles on either side of the head, and are partly enclosed in a dense supporting envelope reinforced with cartilage. The vesicle is filled with a vitreous secretion ; the cells lining its proximal portion form the retina ; the distal portion fuses with an invagination of the surface epithelium to form a composite spheroidal lens, the inner half of which is thus made up of vesicular epitheliuiB, the superficial half of surface epithelium. On either side of the lens the fusion of these two layers forms a doiible epithelial layer — a " ciliary body " — and then the surface epithelium turns upon itself to form an " iris " before 1 Greef, 187.5-77 ; Demoll, 1909 ; v. Hess, 1918 ; Pflugfelder, 1932. « p. 591. 3 See Scarpa (1789), Cuvier (1817), Soemmerring (1818), Krohn (1835-42), Hensen (1865), Schultze (1869), Patten (1886), Carriere (1889), Grenacher (1895), Hesse (1900-2), Merton (1905), Butschli (1921), Alexandrowicz (1927), Heidermanns (1928), and others. 144 THE EYE IN EVOLUTION Figs. 113 and 114. — The Eye of a Typical Cephalopod. e Fig. 113. Invaginated epithelium forms the optic vesicle (a) lined by the retina (b), the posterior layer of the " ciliary body " (c), and the posterior part of the lens (d). The surface epithehum i'orms the cornea (e), the anterior part of the ciliary body (/ ), the iris (t), and the anterior part of the lens (g), a hole (h) being left at the point of invagination. The eye is surrounded by a carti- laginous orbit, formed by an anterior cartilage (k), an equatorial cartilage (I), and an orbital cartilage {m). n is the optic nerve. Fig. — The eye of Octopus vulgaris (specimen from J. Z. Young). THE .Si:\irLE EYE 145 invaginating to line a volummous cul-de-sac extending far posteriorly. Over this the transparent surface epithelium forms a " cornea", sometimes, in Myopsidse, forming a continiiovis layer in which case the cul-de-sac (the " anterior chamber ") is filled with an " aqueous humour " (cuttlefish. Sepia ; squid, Loligo), some- times, in CEgopsidae, perforated by a hole so that the cavity is flushed by seawater (Octopus). The iris is supported by a plate of cartilage and both it and the ciliary body are provided with contractile muscular tissue. The pupil is rect- angular in shape and actively contractile and there is an efficient accommodative mechanism ^ (v. Hess, 1909) ; while covering the iris and extending some distance Sepia is Fig. 115. — The Retina of the Octopus. The retina is composed primarily of a single layer of visual cells with rod-like terminations, r, and nuclei, n. Between the rods and the cell-bodies there is a dark line of pigment, p, and at the proximal extremities of the rods a layer of protective pigment, pp. Most externally there is a layer of nerve fibres, /, with ganglion cells. The white line underneath the pigment is an artefact at the site of a supporting membrane ( X 150) (froin a specimen of J. Z. Young). posteriorly, is a silvery membrane of pavement epithelium which glitters and shines like mother-of-pearl (Figs. 116-17 ; Fig. 192). The retina itself is coiTiprised in the main of visual cells sujDported by two limiting membranes — an internal membrane lining the cavity of the vesicle and an external membrane dividing the retina transversely into two (Fig. 115). The visual cells are made up of two elements, a rod -like termination and a cell -body. The rods lie between the two membranes in palisade arrangement ; they are constricted as they pierce the external membrane, proximal to which lie the cell-bodies with their nuclei, the visual pathway being continued by nerve fibres running in an optic nerve to an optic ganglion.- Prince (1956) described ■)90. p. 52 Loligo -^^ - Octopus S.O. — VOL. I. 146 THE EYE IN EVOLUTION Eledone bipolar cells and ganglion cells in the nuclear layer proximal to the pigmented layer. A considerable amount of pigment is found in association with the visual cells which is most abundant near the narrow neck of the cell between the rod and the cell-body, and in some species at any rate, it is claimed, migrates towards the extremities of the rods in bright light {Eledone — Rawitz, 1891). Such an eye is thus a highly complex organ capable of image-formation and structurally equipped to mediate pattern-vision, able to accommodate over a considerable range and possessed of some power of adaptation. Indeed, in one species, Bafkyteiifhis, the elements of a central retinal area become apparent since Figs. 116 AND 117. — The Pupils of Cephai.opods in Various Stages OF Contraction. Fig. 116. — The pupil of the octopus. Cj Fig. 117. — The pupil of the cuttlefish, Sepia. the rods are greatly elongated as if to form a primitive area centralis, a differen- tiation suggesting the existence of a fixation mechanism endowed with con- siderable visual sensitivity (Chun, 1903). The Inverted Retina A peculiar form of simple eye is associated with an inverted (or inverse) retina, that is, a retina wherein the visual cells are orientated' so that their sensory ends are directed away fro7n the incident light. As a rule, inversion of the retina is associated with a secondary invagination of the optic vesicle. In the usual form of verted (or converse) retina, as we have seen, the cells lining the proximal (deep) portion of the vesicle form the visual cells and their orientation is quite straight- forward ; their receptive elements face the surface and the optic nerve fibres lead directly away from their proximal ends (Figs. 118, 120). In some cases, however, the cells lining the distal (superficial) portion of the vesicle form the visual cells ; since the receptive elements face the inter, of the vesicle, the light must traverse the cell-bodies before it reac.'i the end-organ, and the nerve fibres, issuing superficially, must THE SIMPLE EYE 147 double backwards to reach the o])tic panghon (Figs. 119-121). In such cases the proximal cells of the vesicle usually contain an absorbing pig- ment, and the recejitive ends of the visual cells approximate closely to them, thus reducing the vesicle to a slit-like potential cavity. An arrangement which might at first sight seem anomalous thus acquires a distinct biological value. Moreover, in many species a reflecting crys- talline layer, or tapetum, is found next to the receptive ends of the visual il'l-l-l-l-M-hi' Fig. 118. — The Verted Retina of THE Vesicular Eye. Fir.. 119. — The Inverted Retina of the Vesicular Eye. Fig. 120. — The Arrangement of the Visual Cells in the Verted Retina. Fio. 121. — The Simplest Arrange- ment OF THE Visual Cells in the Inverted Retina. In each case light falls upon the visual cells from above (modified from Buxton, li)12). cells which reflects the incident light backwards so that it traverses the sensory cells a second time thus doubling the intensity for stimulation and incidentally giving the eye a metallic sheen. This arrangement is therefore characteristic of animals to which vision in dim illuminations is important . An inverted retina of this type is typical of Vertebrates but is rare among Invertebrates, being seen in a few Molluscs and Arachnids. Among MOLLUSCS it is found in four species — in its simplest form in the pulmonate, Onchidmm. and in the cockle, Cardium. and in its most elaborate form in two bivalves, the scallop, Pecten, and Spondylus. In the jDulmonate mollusc, Onchidium, the visual cells of a simple vesi- cular eye are inverted and the optic flbres, issuing from their distal ends, pierce the posterior pole of the vesicle in a bundle exactly as does the optic nerve of Vertebrates (Fig. 122) (Semper, 1883). This peculiar eye is also unique in that the " vitreous "' filling the optic cavity is made up of a small number of enormous cells. In Cardium the arrangement of the visual cells is somewhat similar but that of the optic nerve fibres Cardium 148 THE EYE IN EVOLUTION Pecten completely different. The receptive ends of the visual cells lie upon an ectodermal layer of pigment cells crowned by a reflecting tapetum, while their distal ends are prolonged as nerve fibres which run over the retina towards the periphery and then bend backwards circum- ferential ly to form the optic nerve which issues posteriorly. The eye of Pecten is of umisual interest (Fig. 123) ^ ; that of Spondylus is similar.^ A single layer of epithelial cells forms the cornea, underneath this is a clear cellular lens, and posteriorly, separated from the lens by a transverse Figs. 122 and 123. — Inverted Retina in Molluscs. Fig. 122. — The dorsal eye of Onchidium. Showing an inverted retina pierced by the fibres of the optic nerve, resembling the arrangement in Vertebrates. CC, connective tissue forming the cor- nea ; Ep, epithelium ; F, fibrous tissue capsule ; ON, optic nerve ; ONF, optic nerve fibres ; P, pigment layer of the retina ; R, visual cells of the retina ; V, two large vitreous cells (after Glad- stone). O.N. Fig. 123.— The eye of Pecten. C, cornea ; Ep, surface epithelium ; G, ganglion cell layer of the retina ; L, cellular lens ; ON, optic nerve ; P, layer of pigmented cells and above it, the tapetum ; R, layer of rods ; V, cavity of the vesicle ; VS, vascular sinus (after Hesse). Spondylus septum, lies the flattened optic vesicle, the cavity of which has become virtual. The retina itself is complicated. The proximal (deep) portion of the vesicle consists of a single layer of cubical pigmented cells covered by a tapetum ; the more superficial portion of the vesicle consists of two well-defined layers — a proximal layer of rod-like visual elements, the receptive ends of which point posteriorly into the cavity of the vesicle, and a distal layer of cells (the ganglion cell layer of Patten, 1886) through which pass nerve fibres from the visual cells as they run towards the periphery at the equatorial region whence (as in Cardium) they encircle the posterior part of the globe to form the optic nerve (Kiipfer, ' ^ee Keferstein (1862), Patten (1886). Kalide (1888), Carriere (1889), Schreiner (1896). .;psse (1900-2). 2 ■■ Hickson (1882). THE SIMPLE EYE 149 1915). It is interesting that in studying the electrical responses in the eye of Pecten, Hartline (1938) found that the distal layer of the retina mediated a strong off-response while the proximal layer discharged impulses whenever illuminated. In AEACHNiDS, ail inverse retina is seen in the lateral and median posterior eyes of spiders (Araneida), in all the ocelli of pseudo -scorpions (Pseiidoscorpionidea). in the lateral eyes of whip-tailed scorpions (Pedipalpi) and in sea-spiders (Pycnogonida). Each one of these has a Pseudo-scorpion Figs. 124 to 127. — Inverted and Semi-inverted Retin.e in Arachnids. Fig. 124. — The lateral eye of a whip- tailed scorpion. C, cuticular lens ; X, optic nerve fibres ; T, tapetum (after Versluys and DenioU). Fig. 125. — -The eye of a sea-spider. C, cuticle ; Ep, the hypodermal cells, the central ones of which become extremely elongated and surround the retinal cells, V. In the distal part of the eye they give rise to the cells of the lens, L, and in the proximal part, to the tapetum, T. The retinal cells themselves are elongated with a nucleus in the distal part, while the proximal granular part is the sensory receptor. Into these cells the optic nerve fibrils, OX, ramify. The whole eye is surrounded in a pigment cap- sule, P (after Schlottke). Fig. 126. — The lateral eye of a spider. C, cuticular lens ; X, optic nerve fibres ; T, tapetum (after Versluys and Demoll). Fig. 127. — The median eye of a whip- tailed scorpion. C, cuticular lens ; X, optic nerve fibres (after Versluys and Demoll). 150 THE EYE IN EVOLUTION Sea-spider Web spider Scorpion different arrangement. In a further variation, seen in the median eyes of scorpions (Scorpionidea) and in the median eyes of whip-tailed scorpions, the visual cells are doubled upon themselves so that the base of the cell is verted and the sensory end inverted. The simplest arrangement of an inverted retina in Arachnids is seen in the lateral eyes of whip-tailed scorpions (Fig. 124) ; the sensory ends of the inverted visual cells rest on the tapetum, directed away from the incident light, and from the mid-point of the cell-bodies the nerve fibres emerge to run to the periphery whence the optic nerve emerges on the side of the eye (Versluys and Demoll, 1923). A different arrangement again is found in the sea-spiders (Pycnogonids) (Fig. 125). In these, the hypodermal cells secrete a cuticular lens in the anterior part of the eye and a reflecting tapetum in the posterior part. The visual cells are unusually interesting. They are large and triangular in shape, the apex of the triangle lying on the tapetum ; the nuclei are placed distally at the base of the triangle and the narrow proximal ends filled with granular material form the receptive portion of the cell. The arrangement of the optic nerve fibres is unique for they interA^ eave in the substance of the large retinal cells, reaching distally towards the nuclei.^ An ingenious arrangement which probably has optical advantages is seen in the lateral and posterior median eyes of web-spiders : the (anterior) median eyes of these animals have direct, verted retinae (Wid- mann, 1908). In the former the sensory portions of the elongated visual cells point proximally to lie on the tapetum, while the cell-bodies are bent on themselves at an angle of 90°, to run towards the periphery of the retina where the nuclei lie (Fig. 126) ; this portion of the cell does not therefore interpose itself in the path of incident light (Versluys and Demoll, 1923). A semi-inimied retina is found in the median eyes both of scorpions and of whip -scorpions. Here the visual cells, grouped in retinules around rhabdomes, are bent upon themselves at 180°, their nuclei lying proximally next to the tapetum and the receptor ends of the cells being bent round so that their extremities lie alongside the nuclei : here again there is the optical advantage that the incident light does not travel through the bases of the visual cells (Fig. 127) (Scheuring, 1913 ; Versluys and Demoll, 1923). It will be remembered that the subepithelial eyes seen most typically in platiarian and nemertine worms ^ wherein the visual cells dip downwards from ' ; [organ (1891), Korsehelt and Heidei- (1893), Bouvier (1913) Schlottke (1933). " P 134. Wiren (1918), THE SIMPLE EYE 151 the surface into a cup of pigmented cells, and the conducting prolongations of the cells are turned towards the direction of the incident light, have the con- figuration of an " inverted "' retina. In a sense, also, the composite simple eyes of Chsetognaths and some of the smaller Crustaceans to be discussed immediately are also of this type. AGGREGATE EYES The AGGREGATE EYE is a Suitable name to designate an accumu- lation of ocelli so closely packed that they bear a superficial resemblance to a compound eye although each is anatomically separate. Such an arrangement is seen in its most simple form in starfishes (Plate I), in such insects as the male Stylops ^ or in Myriapods (Fig. 210),^ in which it appears as a cluster of ocelli. Stylops Figs. 128 and 129. The Aggregate Eye of Braxchiomma yEsicctoscM. Fig. 128. — Cross-section through a branchial fila ment of the worm. BV, blood vessel ; C, cuticle F, fibril ; L, lens ; X, nucleus ; visual cell (after Hesse). Fig. 129. — Axial section through two ocelli. Car, cartilage ; Cil, cilia ; Ep, epidermis ; ON, optic nerve ; P, pigment cells ; R, An entirely difTerent type of aggregate eye is seen in the branchial filaments of some sedentary polychsete worms and in certain lamelli- branch molluscs wherein the organ has a superficial structural resem- blance to a compound eye but each element contains only one sensory cell (Figs. 175-6). In the first case, the eye of the polychsete, Branchiomma vesiculosum, is made ujd of a spherical group of elements resembling ommatidia, but since each contains only a single cell it should be considered an ocellus and the eye is technically a simple organ of the aggregate type (Brunotte. 1888 ; Hesse, 1896-99) (Figs. 128 and 129). It is to be remembered, however, that in such tube-worms these structures do not seem to be essential for the animal's characteristic response to changes in light intensity (Millott, 1957). A similar arrangement is seen in the eyes of the lamellibranch molluscs. Area and Pechmcidus (Carriere, 1885 ; Patten, 1886 ; Hesse, 1900). Branchiomma 221, ' P- 110. 152 THE EYE IN EVOLUTION COMPOSITE OCELLI COMPOSITE OCELLI (SIMPLE EYEs) are formed by the fusion of two or more ocelli each with its own retina and pigment cnp, a process which seems to have arisen independently in several phyla ; in Figs. 130 to 132. — The Composite Ocellus. Cypris Fig. 130. — The ocellus of Cypris. Fig. 131. — The ocellus of Daphnia. The unpaired median eye represents the fusion of 3 ocelli (see Fig. 228). DL, dorso-lateral ocelli; VE, ventral ocellus; P, pigment mantle; V, visual cells; T, tapetum (after Claus, 1891). EDIAL VENTRAL Fig. 132. — The ocellus of the chsetognath, Spadella exaptera. Showing 3 of the 5 simple eyes, one to the left and 2 to the right, arranged round the central pigment, P. Ep, epithelium ; V, visual cells ; R, rods ; N, nerve fibres (after Hesse). general, the fusion is associated with degeneracy and lack of use. It is interesting that the same cyclopic tendency is seen in the median (pineal) eye of Vertebrates, which initially was a paired organ. ^ Among certain smaller Crustaceans, lowly types which have undergone much reduction of the head and have largely lost their segmentation, a median unpaired eye is a characteristic feature, and is frequently composed of the fusion of a number of ocelli arranged in a somewhat similar way (the Cladoceran, Daphnia ; the Ostracods, Cypris and Cypridina ; the Copepod, Cyclops) (Figs. 130 and 131). ^ Among the marine arrow-worms (Chsetognatha), Spadella has two composite ocelli near the anterior extremity of its body, each organ made up of the fusioi! >f 5 simple eyes of the cupulate type arranged around a central Cyclops 1 p. 711. p. 163, Fig. 145. THE SIMPLE EYE 153 mass of pigment which sends out partitions between each (Fig. 132) (Hesse, 1908). In such eyes the receptor ends of the sensory cells are directed inwards towards the cup of pigment, and the nerve fibre is peripheral so that the eye may be considered as of the inverted type (Vaissiere, 1955). Alexandrowicz. Arch. Zool. exp. gen., 66, 76 (1927). Berger. J. comp. Xeurol. Psychol., 8, -23 (1898). Berger and Conant. Johns Hopk. Univ. Circ, Baltimore, 18, 9 (1898-99). Bhatia. Nature (Lond.), 178, 420 (1956). Bolwig. Vidensk. Medd. Dansk. naturh. Foren., 109, 81 (1946). Bonnet. Oewi'res, Neiichatel (1781). Bouvier. Deu.xihne exped. antarctiqite frang., Paris, 1 (1913). Brunotte. C.R. Acad. Sci. (Paris), 106, 301 (1888). Biitschli. Vorlesungen iiber vergl. Anat., Berlin, 817, 826, 872 (1921). Buxton. Arch, vergl. Ophthal., 2, 405 (1912). Carriere. Die Sehorgane der Tiere, Miin- chen (1885). Arch. mikr. Anat., 33, 378 (1889). Chun. Verhdl. dtsch. Zool. Ges., 13, 67 (1903). Cuenot. Grasse's Traite de Zool., Paris, 6, 13 (1949). Cuvier. Alew. pour servir a Vhistoire et a Vanntomie des mollusques, Paris (1817). Demoll. Zool. Jb., Abt. Anat., 27, 651 (1909). Galati-Mosella. Monit. Zool. Hal., 26, 75 (1915); 27, 161 (1916); 28, 129 (1917). Greeff. Sitz. Ges. Beforderung Gesammt. Naturw. Marburg, 115 (1875). Nova Acta Leopoldina, 39, 33 (1877). Grenadier. Zool. Anz., 18, 280 (1895). Hartline. J. cell. comp. Physiol., 11, 465 (1938). Heidermanns. Zool. Jb., Abt. Zool. Physiol., 45, 609 (1928). Hensen. Z. wiss. Zool., 15, 155 (1865). Hertwig. Das Nervensysteni ii. die Sinnes- organe der Medusen, Leipzig (1878). Die Zelle und die Gewebe. Jena (1893). V. Hess. Arch. Augenheilk.. 64, Erg., 125 (1909). Pflilgers Arch. ges. Physiol., 122, 449 (1918). Hesse. Z. uiss. Zool., 61, 393 (1896) ; 62, 671 (1897) ; 63, 361 (1898) ; 65, 446 (1899) ; 68, 379 (1900) ; 72, 565 (1902). Das Sehen der )iiederen Tiere, Jena (1908). Hickson. Quart. J. micr. Sci., 22, 362 (1882). Imms. Textbook of Entomology, London (1935). Jourdan. Les sens chez les animaux infer ieurs, Paris (1889). Kalide. Zool. Anz., 11, 679, 698 (1888). Keferstein. Z. wiss. Zool., 12, 133 (1862). Korschelt and Heider. Vergl. Entwicklung. d. Wirbellosen Tiere, Jena, 664 (1893). Krohn. Nova Acta Acad. Leop. -Carol., 17, 337 (1835) ; 19, 41 (1842). Kiipfer. Viertlj. naturf. Ges. Zurich, 60, 568 (1915). Maier. Zool. Jb., Abt. Anat.. 5, 8, 552 (1892). Merton. Z. u-iss. Zool.. 97, 341 (1905). Millott. Endeavour, 16, 19 (1957). Morgan. Biol. Stud. Johns Hopk. Univ., 5, 49 (1891). Patten. Mitt. zool. Stat. Neapel, 6, 568 (1886). Pfliigfelder. Z. wiss. Zool., 142, 540 (1932). Prince. Texas Rep. Biol. Med., 13, 323 (1955). Comparative Anatomy of the Eye, Springfield, 111. (1956). Rawitz. Arch. Anat. Physiol. {Physiol. Abt.), 367 (1891). Scarpa. Anatomical disquisitiones, Ticini (1789). Scheunng. Zool. Jb.. Abt. Anat., 33, 553 (1913). Schlottke. Z. mikr. Anat. For.sch.. 32, 633 (1933). Schreiner. Die Augen bei Pecten u. Lima, Bergons Museum Aarbog (1896). Schultze. Arch. mikr. Anat., 5, 1 (1869). Semper. Int. Sci. Ser.. 31, 371 (1883). Soemmerring, D. W. De oculorum hominis aniynaliumque etc., Goettingen, 76 (1818). Vaissiere. C. R. Acad. Sci. (Paris), 240, 345 (1955). Versluys and Demoll. Ergebn. Fortsch. Zool., 5, 66 (1923). Whitman. J. Mor;j/io/., 2, 586 (1889). Zool. Jb., Abt. Anat., 6, 616 (1893). Widmann. Z. wiss. Zool., 90, 258 (1908). Wigglesworth. Parasitology, 33, 67 (1941). Wiren. Zool. Bidrag Uppsala, 6, 41 (1918). 154 THE EYE IN EVOLUTION Fig. 133.— Johannes Muller (1801-18.18). The Compound Eye Nothing could be more suitable to introduce this section on the anatomy and physiology of the compound eye than the portrait of Johannes mxjllee (1801-1 :-^s (Fig. 133), Professor of Physiology first at Bonn and then at Berlin, a studeii friend and collaborator of von Helmholtz. In association with Malpighi , Haller, he may be considered the fovmder of the great German School of . -iology of the 19th century. Throughout his relatively short THE COMPOUND EYE career he contributed lavishly to many branches of biology but perhaps the conception for which he is best remembered is the law of specific yierve energies which lays down that each organ, however stimulated, gives rise to its own characteristic sensation. ^^ His enunciation of the Mosaic Theory to explain the optical properties of the compound eye has stood the test of time, and was the first scientific explanation advanced on this subject ; Fig. 156 is a characteristic illustration from his book. His classical textbook on human physiology - crystallized the knowledge of his day in a vast compendium which stimulated work in every field for more than one generation. The compound eye, an organ peculiar to Arthropods, has evolved along different lines from the ocellus. In the former, instead of being independent of each other, the sensory elements are structurally and fnnctionaUy associated in groups. For this purpose complexity has been attained by the division of the indi^•idual sensory cells of a simple 155 Fig. 134. — The Compound Eye. Diagram of a compound eye of an insect with a sector excised. a, corneal facet ; h, crj'stalline cone ; c, surface epithelium ; d, matrix cells of cornea ; e, iris pigment cell ; /, cell of retinule ; g, retinal pigment cell ; h, rhabdome ; ;', fenestrated basement membrane ; _;, nerves from retinular cells ; k, lamina ganglionaris ; /, outer chiasma. eye to form a coordinated colony, a process first shown to occur in the development of the stalkefl eyes of the shrimp, Crangon, by Kingsley (1886) and confirmed by others in many different species. Moreover, optical imagery has been attained not by the single large lens charac- teristic of the ocellus (or of the vertebrate eye) which by attaining an adjusting mechanism reached its highest development in Cephalopods, but by ensheathing each individual group with pigment, thus convert- ing the eye into a series of blackened tubes so that the multiplicity of images increases the acuity of vision by a mosaic effect. In this arrangement each separate element is called an ommatidium {ofifnx, ' Zur veryleicheiulen Physiologie
1.5.5. — Superposition Images formed by the Refractive System of LAMpyjtis. Fig. 154. — The mosaic of images Fig. 155. — The superimjiosed images formed at a level immediately be- at the level of the rhabdome (after neath the optical system. Exner). The functional contrast between the two types is seen in Fig. 153. In Figs. 154 and 155 are seen the illustrations from Exner's (1891) classical treatise showing the image of a candle flame formed by the corneal facets and cones of the fire-fly, Lampyris. When the microscope is focused just below the dioptric apparatus a multitude of luminous spots is seen all of which become merged into one at the level of the rhabdomes. The light from as many as 30 different facets may thus be concentrated on one of these structures. Intermediate forms between these two types of compound eye exist ; nor are they mutually exclusive. Thus in Mantids the two are seen combined in the same eye ; the anterior ommatidia which are used for binocular vision are of the apposition t^'pe while the lateral parts are of the superposition tyjDe (Friza, 1928) — a functionally efficient arrangement. Moreover, as in Crustaceans, the change from a superjDosition eye of the nocturnal tyjje to an apposition eye of the diurnal type with its high degree of resolution can be made functionally 1 p. 173. Fire-fly 170 THE EYE IN EVOLUTION Butterfly ( Vanessa) by a migration of pigment, thus effecting an adaptive process in species which are active both by day and by night : in dim hght the pigment becomes concentrated anteriorly so that the eye can function as a super- position eye and make full use of all the available light ; while in bright illumination it disperses and migrates posteriorly surrounding each retinule with an opaque mantle intercepting all lateral rays (Parker, 1932). Thus in the dark-adapted state examination of the eyes of certain noctuid moths with an ophthalmoscopic mirror shows a luminous red reflection from a group of ommatidia ; in the light - adapted state there is a minute glow from one central ommatidium only (Demoll, 1917 ; Horstmann, 1935). This pigmentary migration in some butterflies and moths begins from half to one hour before sunrise or sunset and the change occupies an interval varying from r. few minutes to an hour (Merker, 1929-34 ; Collins, 1934). The excised eye always adopts the light-adapted distribution of pigment. The migratory response is abolished by narcosis nor does it occur in butterflies when the insect is at rest and inactive (Demoll, 1909-11 ; Day, 1941). Its mechanism is unknown ; a purely hormonal control is improbable since individual ommatidia may respond to localized illumination (Day, 1941) ; but whether the migration of pigment is dependent upon nervous reflexes from the retinule or is initiated by photochemical reactions within the pigmentary cells is controversial. Notonecta Pigmentary migration of a less dramatic kind occurs in certain purely apposition eyes of diurnal species as a response to rapid changes in illumination. These are associated chiefly with the pigment in the cells around the basement meinbrane (butterflies — Demoll, 1909 ; the water-boatman, Notonecta — Bedau, 1911). In the latter the visual cells also elongate in the dark-adapted state (Liidtke, 1951-53). The Optical System of the Coni2)ound Eye The optical system of the compound eye has always excited considerable interest since it was first studied by Johannes Miiller (1826) ; Fig. 156, taken from his classical work on^ this subject, indicates characteristically his conception of the optical mechanism whereby a point source of light excites only one (or two) ommatidium. In his Mosaic Theory he showed that an image of considerable definition would be formed by the juxtaposition of the many small luminous stimuli received by the ommatidia, each of them the impression of the corresponding projection in the visual field, each of them varying acocjrding to the pattern of the incident light. Such an image, in CO])- r?) distinction to that formed by the eye of Vertebrates, is erect, and the -f can be easily simulated by allowing light to traverse a bundle of Dj tubes and fall upon a plate of ground-glass, an arrangement THE COMPOUND EYE 171 which clearly shows that the definition of the image depends on the number of tubes per unit area (Alverdes, 1924). Using the excised anterior segment of the eye of the fire-fly, Lampyris, as a lens, Exner (1891) succeeded in photographing the image (Fig. 157) ; the degree of resolution thus obtained has been estimated by Marchal (1910) to Fig. 156. — The Compound Eye According to Johannes Muller. When light emitted by different points, a, b, c, d, falls on the ej^e, that from a completely illuminates cone e, but the ommatidia to the right of e are not illuminated all the way down. Only the nerve /, issuing from cone e, is thus stimulated by the source a, while light from the same source entering other onimatidia is unable to stimulate the fibres since it is absorbed by the pigment sheaths. Similarly, light from b, stimulates two ommatidia at/ ; light from c, two ommatidia at g ; and light from d, one ommatidium at h (from Miiller, 1826 ; by permission of the Cambridge University Library ; by courtesy of Dr. Pirenne and the Pilot Press). correspond approximately to an acuity of 1/60 in the human eye. It is important to realize that owing to the isolating effect of the pig- ment mantle, no formed image is produced at the level of the receptor cells ; each of these acts only as a photometer and from the mosaic thus formed by the individual ommatidia the picture of the outside world is synthesized in the central nervous system (van der Horst, 1933). 172 THE EYE IN EVOLUTION Musca Dragonfly Necrophorus Apis In the compound eye of the winged male of Lam2Jyris there are 2,500 ommatidia ; but the number of elements varies considerably between different species depending largely on their habits. Thus, in Solenopsis, the worker-ants which live underground have 6 or 9, while the winged males which pursue the female in tlie air are provided with 400 ; in genera with a high visual acuity the numbers are much higher — in the house-fly, Musca, 4,000 ; in the water-beetle, Dytiscus, 9,000 ; and in dragonflies (Odonata) up to 28,000 (Demoll, 1917 ; Imms, 1935), or the burying beetle, Necro- phorus, 29,300 (Leinemann, 1904). The size of the individual facets re- mains fairly constant (15 to 40/x) ; the size of the eye is determined essenti- ally by their number. From the functional point of view, however, the most important feature is the ommatidial angle. that is, the angular extent of the visual field covered by each element. It is obvious that if a pattern is to be resolved, two adjacent ommatidia must be unequally stimulated so that their angular separation must form the anatomical basis of the visual acuity, corresponding in man to the inter-cone distance and determining the fineness of the " grain " of the resulting picture (del Portillo, 1936). As this angle becomes smaller, the resolving power increases, but less light will enter each facet. Thus the angle in the bee. Apis, varies from 0-9° to 1° in the centre of the eye, and in the earwig, Forficula, is 8°, so that the latter will obtain a single point of light as the image of an object which the eye of the bee will resolve into 64 (Baumgartner, 1928 ; V. Buddenbrock, 1937). In the locust, Locusta, the ommatidial angle is about 21° (Burtt and Catton, 1954). In the periphery of the eye the ommatidial angle is larger than in the centre and the acuity corres- pondingly less; in the anterior region of the eye it is often smaller than in i ' ventral, an arrangement which favours visual acuity in flight (Aut. jiu, 1949) (Fig. 158). Fig. 157. — Exner's Classical Photo- graph THROUGH THE OPTICAL SYS- TEM OF THE Compound Eye of Lamp mis splesdidula. Showing a window with a letter R on one pane and a church beyond (from Wigglesworth's Principles of Insect Physiologu, Methuen). THE COMPOUND EYE 173 Exner's early work on the dioptrics of the ommatidial system still remains classical. He showed that the essential refractive device is the crystalline cone, which, of course, vmlike the lens of Cephalopods and Vertebrates, has a fixed focus incapable of adjustment. The crystalline cone itself is composed of concentric lamellae the refractive index of which increases progressively from the perii^hery to the central axis (Fig. 159) ; it therefore acts as a " lens-cylinder " wherein an obliquely incident ray is progressively refracted until it is gradually Forficiila Fig. 158. — The Ommatidial Angles of the Eye of the Honey-Bee. The ommatidia are drawn in groups of 3, and the drawing shows the way in which an ommatidial angle varies in different parts of the eye ; the values of the angles are given in degrees (Pirenne, after Baumgartner). brought back to the axis. It is probable that the crystalline cone thus brings the image formed bj^ an ommatidimn to a small point although different wave- lengths will be brought to a focus at different places (Goulliart, 1953). To some extent therefore, the optics of the comjaoand eye with its many elements is comparable to the analysis made by television. The appositional eye wherein the retinule abuts against the crystalline cone may be compared oj)tically to such a system wherein rays of light pass through a lens-cylinder of a length equal to its focal distance (Fig. 160). In this event a beam of parallel light (mpn) entering perpendicularly to one edge of the cylinder (ab) will be focused as an inverted image at y on the other edge and will Locust a 174 THE EYE IN EVOLUTION b Fig. 159. — The Lens Cone of THE Compound Eye. The laminated optical structure of superimposed la- mellae (after Exner). emerge as a diverging beam (m' p' n'). Oblique rays (g) will emerge at an angle as q' . The pigment mantle around the cones, however, will absorb oblique rays and virtually permit the light to emerge only at y, where the image falls as a single luminous point on the subjacent retinule ; the apposition of all such points will form the complete erect image perceived by the eye. In the superpositional eye, on the other hand, the optical system will correspond to a lens-cylinder of a length equal to twice its focal distance (Fig. 161). The inverted image of a distant object will be formed in the middle of the cylinder {xy) ; the rays traversing the remaining half of the cylinder will pursue a symmetrical course and emerge at an angle (^) equal to that at which they entered (a) but opposite in direction. Not only will normal rays thus fall on the distant rhabdome but also oblique rays refracted from the cones towards the same side from which they have come, so that a number of separate images can be super- iinposed on one visual element. The resultant image thus gains in luminosity at the sacrifice of resolution. The ability to analyse the plane of polarized light is a common function of the compomid eyes of Arthropods and of both the simple and compound eyes of Insects ; it is a function which is freely used to aid orientation out-of-doors.^ The structure which serves as an analyser, however, has given rise to controversy. The suggestion that Fig. 160. — The Optical System of THE Apposition Eye. The i; u^ cylinder is equal in length to its foe- distance (after Exner). Fig. 161. — The Optical System of THE Superposition Eye. The lens cylinder is equal in length to twice its focal distance (after Exner). 1 p. 66. See Kalmus. Nature (Lend.), 184, 228 (1959). THE COMPOUND EYE 176 the retinular cells act as differentially orientated detectors ^ was based on differences in the electrical response with variations of the direction of polarization of the incident light. Such a suggestion, however, is difficult to accept if it is agreed that the individual cells are not furnished with corresponding axonal transmission ^ ; the theory could not be made to adapt itself to the proven single impulse transmitted from each entire ommatidium in the eye of Limulus (Waterman, 1950; Waterman and Wiersma, 1954) ; moreover, such a change does not seem to be invariable.^ It has also been suggested that the ultra- structure of the rhabdome with its composite laminated and fenestrated bodies, could provide a physical basis for this faculty (Fernandez- Moran, 1956). An alternative hypothesis is that the responsible structure is the corneal facet with its chitinous covering which is birefringent, rather than any structure within the ommatidium (Waterman, 1951 ; Berger and Segal, 1952). Wolsky (1929) and Stockhammer (1956), however, were unable to detect any optical mechanism which could act as an analyser in the entire dioptric apparatus in the insects which they studied, and concluded that this mechanism resided in the visual cells. It is obvious that further research is required on this problem, and it may well be that more than one mechanism is operative, differing in different species, or a mecha- nism as yet unsuspected. Alverdes. fii'o?. Z6Z., 43, 577 (1924). Biitschli. Vorlesungeniiber vergl.Anatomie, Ast. Zool. Jb., Abt. Anat., 41, 411 (1920). Berlin, 872 (1921). Autrum. Exjjerientia, 7, 271 (1949). Cajal and Sanchez. Trab. Lab. Invest. Autrum and Gallwitz. Z. vergl. Physiol., biol. Univ. Madrid, 13, 1 (1915). 33, 407 (1951). Rev. chil. Hist, nat., 25 (1921). Autrum and Stumpf. Z. Xafurjorsch., 5b, Chun. Bibl. Zool., 7, 193, 213 (1896). 116 (1950). Claus. Manuale de Zool., Milano (1879). Baumgartner. Z. vergl. Physiol., 7, 56 Collins. J. ex;;. 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CHAPTER VII THE SYSTEMATIC ANATOMY OF INVERTEBRATE EYES From the morphological point of view we have seen that the visual organs of Invertebrates show an astonishing range in structure, varying in complexity from the simple eye-spot or the single visual cell to the elaborate organs characteristic of Cephalopods or Insects ; from the functional point of view the variation is equally great, evolving from a primitive and j^erhaps undifferentiated sentiency which may influence metabolic and motorial reactions, to the capacity to form elaborate images whereby intensity, hue, form and spatial relationships can be differentiated with sufficient exactitude and appreciation to determine behaviour. The curious thing, however, is that in their distribution the eyes of Invertebrates form no series of contiguity and succession. Without obvious phylogenetic sequence, their occurrence seems haphazard ; analogous photoreceptors appear in unrelated species, an elaborate organ in a primitive species ^ or an elementary structure high in the evolutionary scale, ^ and the same animal may be provided with two different mechanisms with different spectral sensitivities subserving different types of behaviour. A striking example of this is seen in the flat-worm, Planaria lugubris, which has both positive and negative photo -reactions (Viaud and Medioni, 1949) ; if this aniinal is bisected the photo -positive reactions appear in the posterior segment before the nerves regenerate suggesting that these responses are due to dermal sensitivity, while it has been shown that the photo -negative reactions are due to the eyes ; photokinesis is dependent on the skin, positional orientation to light on the eyes. In the earthworm, Lurnbricus terrestris, on the other hand, the photo-negative reactions in bright light are controlled by the head -ganglion, while the photo-jDOsitive reactions in dim light are nnediated by ; the ventral cord ; the two activities are mutually antagonistic but normally the cephalic mechanism is dominant (Prosser, 1934). Again, the possession of both ocelli and compound eyes by many insects, the first sometimes reacting to polarized light and orientative in function, and the second to ordinary light as well and also subserving form vision, is an example of two mechanisms which are supplementary in function and not antagonistic (Wellington, 1953). We shall now discuss the occurrence of these organs in the inverte- brate phyla, referring back to the previous chapter for a description of their ii: nute structure. ^ Such as the complex eye of the jelly-fish, Charybdea (p. 183). Such as the simple eyes of Insects (p. 224). TYPICAL PROTOZOA [Drawn not to scale, but approximately to a starulard size.'] SARCODINA 179 A mceba Foraminifei Radiolariaii shell FLAGELT.ATA Euglena Trypanosoma Trichomonas Xoctiluca (see Fig. 886) Gonyaulax (Dinoflagellate) Paramcpcium Vorlicella SPOROZOA Suctorian Sporozoite of Plasmodium 180 THE EYE IN EVOLUTION Protozoa PROTOZOA are the most primitive and simplest of animals, some of which might with equal justification be considered as plants ; they are essentially single-celled but sometimes form loose colonies by budding or by cell-division, showing some degree of co-ordination but never forming differentiated tissues. Of all animal types they are the most numerous, being found in every continent, on land, in fresh water, in the seas and impartially distributed as parasites within all animals (including some of their own kind), among which not the least fre- quented is Man ; their skeletons contribute largely to the oozes of the seas and to the composition of the rocks of which the land-masses are made. Within the phylum four methods of activity are evident — amoeboid movement, flagellate and ciliary progression, and encystment with spore -formation, characteristics under which the upwards of 15,000 species may be conveniently grouped into 4 classes (see p. 179). SABCODiNA (or rhizopoda), Organisms which progress by sending out finger-Hke pseudopodia into which the protoplasm of the cell pours itself. This class comprises such types as the fresh -water Amoeba, the parasitic Entamceha or the marine Foraminifera with chalky shells and Radiolaria with siliceous shells which after death enter largely into the formation of the oozes of the bed of the ocean. FLAGELLATA (or mastigophora), Organisms which swim by the lashing movements of one or a few whip-like flagella. The class comprises such types as the common Euglena and colonial forms such as Volvox almost universal in fresh-water ponds, the parasitic, disease-producing Trypanosomes and Tricho- monads, Dinoflagellates including Noctiluca which gives luminescence to the seas,^ and Cystoflagellates, important constituents of the plankton of lakes and the oceans. ciliophora, organisms which progress by the coordinated movements of many hair-like cilia. The class comprises the Ciliates (such common types as the slipper-shaped Paramoscium, the bell-shaped Vorticella or the trumpet- shaped Stentor) and the Suctorians which lose their cilia in adult life and in their place develop tentacles used as suckers by which they capture and suck out the bodies of their protozoan prey. sporozoa, encysted organisms without a locomotive mechanism ; they are parasitic on almost every species of animal and are spore-forming in habit (Coccidia, Hsemosporidia, Plasmodium, etc.). In view of the fact that the response to light in these primitive forms is motorial, it is not surprising that receptors are not found in the passive parasitic Sporozoa ; in the first three classes responses to light are found among the freely-swimming active types, but as would be expected in imicellular organisms, the receptor mechanisms are of the most pr i itive nature. In the Sarcodina (Amceba) and some Ciliates 1 p. 738. PARAZOA 181 {Paramoecmm) sensitivity to light is diffuse ; in other Cihates {Stentor) it is localized to a part of the organism but without apparent specific mechanism ; but even at this primitive unicellular stage an obvious localization of function may be attained by the development of an EYE-SPOT and the efficiency of the organelle increased, particularly in the acquirement of a crude directional appreciation, by the provision of pigment (as in Euglena) ^ or even of a primitive refractile mechanism (as in some Dinoflagellates).^ Parazoa The SPONGES (porifera), sessile marine animals which form living thickets in the sea, represent a cul-de-sac in evolution between Protozoa and Metazoa dating back almost to the beginning of geological records. They are the simplest multicellular animals and show the beginnings of the development of a "" body " composed of tissues ; but although there is cellular differentiation there is little cellular co-ordination. Being vegetative and sedentary in habit they have no need of sense- organs as they lie moored to rocks or sea-weed. They possess no nerve cells but the body cells retain properties of an irritability of a low level ; and in the active larval forms of certain types (the simple sponge, Leucosolenia) apolar light-sensitive cells of the most elementary type have been described (Minchin, 1896). Invertebrate Metazoa In Metazoa — which includes all animal species apart from the Protozoa and Parazoa — -the development of specialized cells and their eventual co-ordination into distinct organs allow the evolution of specific sensory activities as the term is generally understood. These we shall now study, but it must be remembered that the Invertebrates (or Non-chordates) do not form a homogeneous sub-kingdom but rather represent an assemblage of unrelated groups of animals which have little in common except the negative attribute of not being provided with a dorsal nerve-cord with its supporting axis or with gill-slits. From our restricted point of view there is the dramatic diff"erence that (with few exceptions) the eye when present is developed from the skin, while in Vertebrates it originates as an outgrowth of the brain. cgelexterata CCELENTERATES are simply formed animals with a body-cavity (coelom) and digestive cavity(enteron) combined so that the body is formed as a sac with an opening at one end only. They show the beginnings of separate organs witli a consequent division of labour, and among them Leucosolenia Sycon 126. - p. 126. 182 THE EYE IN EVOLUTION Hydra Obelia medusoid Obelia polyp Sea-anemone Comb jelly (see Figs. 887-8) visual structures of some complexity first make their appearance. The phylum may be divided into two sub-phyla — the cnidaria, provided with numerous stinging cells (kvlSy), a nettle), and acnidaria, wherein these are replaced by adhesive cells. The first-sub-phylum is divided into 3 classes : HYDROZOA, comprising solitary polyps such as tlie fresh-water Hydra, the marine Hydroids, branching colonial polyps of vegetative appearance liberating freely-swimming Hydromedusie {Obelia, Sarsia, etc.) and some j^elagic colonial forms. SCYPHOZOA (" cup animals "), marine jellyfish, free-swimming medusae, typically umbrella-shaped with the important organs situated on the margin or under-surface. ANTHOZOA (" flower animals "), sessile marine polyjas with no medusa- forms, such as sea-anemones, sea-fans, sea-pens and corals. ACNIDARIA, comprising the Ctenophnra (comb-jellies or sea-gooseberries), delicate freely-swimming globular organisms, pelagic in habit, gelatinous and transparent, beautifully iridescent in the sunlight and often luminescent in the dark,^ provided with comb-like rows of cilia. The degree of elaboration of the visual receptors varies with the motility of the organism, and many Coelenterates are sessile, plant-like zoophytes ; eyes are therefore confined to the mobile medusae and these are of a very primitive nature,^ while the sessile polyps of this phylum (hydroid forms and all Anthozoa) have no sense organs or, at most, contact photoreceptors of the most elementary type.^ The Ctenophora are provided with a sense organ at the upper pole of the organism consisting of a mass of limestone particles sup- ported on cilia associated with sensory cells communicating by nerve fibrils with the swimming-combs; this is considered to act as a statocyst or balancing device and visual organs are absent. Among the Hydrozoa, some fresh-water forms are sensitive to light but possess no detectable visual organs ; a hydra, for example, will migrate towards the lighted side of its container where, incidentally, there are usually more food-organisms. In some freely-swimming Hydromedusae, however, externally visible light-sensitive organs provided with sensory cells and pigment and sometimes a refringent appara- tus may be found in the tentacular bulbs at the bases of the tentacles (Fig. 162) ; these take the form of ' p. 739. ^'ir detailed information, see O. and R. Hertwig (1877) Ber^ S98), Linko (1900), v. Uexkull (1909), Lehmann (1923). il6. Fig. 162.— The Medusoid Form OF BoviiAi.sriL- LEA (Margel/.s). M, manubrium; R, radial canal ; S, sense organ (after Allman). Schewiakoff (1889), CCELENTERATA 183 a primitive fiat eye, as in Turris or Lizzia (Fig. 96), or are invaginated as an elementary cupulate eye, as in Sarsia (O. and R. Hertwig, 1878 ; Jourdan, 1889). These organisms are light-sensitive and extirpation of the tentacular bulbs with the ocelli completely abolishes the response to light. Among the jellyfish (Scyphozoa) more elaborate organs are seen. In the common jellyfish. Aurelia aurita, which is found in great shoals around the British coast, eight sense-organs (tentaculocysts) arise as modifications of tentacles ; each, lying in the protection of a marginal Figs. 163 and 1(54. — The Common Jellyj^sh, Acrelia aurita. Fig. 163. — Side view of the jellyfish, showing the numerous marginal tentacles hanging from the border of the convex umbrella, and the dependent oral arms. The margin of the umbrella is broken by 8 notches, the marginal lappets (L). Fig. 164. — A marginal notch, showing a ten- taculocyst comprised of two olfactory pits, OP, a calcareous concre- tion, C, and an ocellus, OC (modified from Lankester). niche, has three types of sensory cells — red or black pigmented cells responding to light, " olfactory " cells with a chemical appreciation, and club -like cells containing calcareous concretions with a balancing function (Figs. 163-4). Exceptionally, as in the Cubomedusan, Charybdea, a large ocellus has been reported with a cellular lens, a vitreous structure and a complex retina — an organ structurally capable of some degree of visual imagery (Fig. 102) (Schewia- koff, 1889 ; Berger, 1898). The biological value of this elaboration in a brainless organism is somewhat speculative. ECHINODERMATA Among ECHiNODERMS (" spiny skinned "), a phylum characterized by its radial symmetry, visual organs are rudimentary. This would 184 THE EYE IN EVOLUTION Starfish Brittle-star be anticipated from the absence of centralization in the nervous system, associated presumably with the absence of a head region, and from the characteristically sluggish and sedentary habits of its members. The phylum is divided into 5 extant classes : ASTEROiDEA, or starfishes, motile but sluggish organisms. OPHiUKOiDEA or brittle-stars, resembling starfishes but with the arms sharply marked off from the central disc. ECHINOIDEA or sea-urchins, living off rocky coasts, with a round pin- cushion-like body covered with plates and provided with long sharp spines. HOLOTHUEOiDEA Or sea-cucumbers, worm-like creatures with calcareous plates, occurring in most seas. CRiNOiDEA, sea-lilies or feather-stars, stalked forms anchored on rocks or Free-swimming feather-star Fig. 165. — The Iridophokes ix the .Sea-urchin, Djadema aatjllarum. Section through a cluster of iridophores, I ; E, epidermal layer ; M, melanophores, underneath which lies the superficial nerve layer (fixed Bouin ; stained Masson's argentaffine reaction ; counter-stained Mallory's triple stain. (Approx. X 500) (N. Millott). in mud usually at great depths, with appendages (cirri) and branching arms growing from a central cujd ; feather-stars become free-swimming in adult life. In most Echinoderms the skin is diffusely sensitive to light, particularly in sea-cucumbers (Crozier, 1914-15) ; in brittle-stars and feather-stars there are no special sense organs ; in sea-cucumbers sense organs are represented by statocysts sometimes present at the bases of the tentacles, and tactile processes sometimes present on the dorsal surface of some of the creeping forms ; " eyes " are present only in starfishes. The diffuse dermatoptic sense shows interesting variations. Thus in some starfishes the body-surface is said to be sensitive to changes in intensity, the podia and skin gills to steady light ; in some sea-cucumbers {Synapta) the whole sn; •■■ is sensitive to both, while in others {Holothuria surinamensis) the rim of the •■'' ica is particularly sensitive, the posterior end and tentacles less so and the ) ia least. In the sea-urchin, Paracentrotus lividus, the apical poles are ECHINODERMATA 185 Fig. 166. — Diagram of a Very Young Asteroid At the base of the 5 terminal tentacles is an optic cushion with a bright red ocellus, Oc, connected by an epidermal radial nerve which runs to the central nerve pentagon surrounding the mouth (after Lang). Compare Plate I. said to show the most rapid reactions (Scheer, 1956). In the Echinoid, Diadema, the distribution of sensitivity corresponds to the distribution of the nerve elements and it may be that these are directly stimulated bj- light as we have seen to occur in the apolar light-sensitive cells of w- orms (Millott, 1954). On the other hand, photosensitive pigments may be present in minute quantities, but there is yet no evidence as to their nature. Many sea-urchins have the same primitive sensitivity associated particu- larly with their pigmented spicules which move on the stimulus of light (v. Uexkiill, 1900), and in some types characteristic iridescent bodies associated with melanin pigment lie near the spines {Diadema antillarutti) (P. and F. Sarasin, 1887 ; Dahlgren, 1916; Millott, 1950-54). These represent clusters of regularly arranged plates resembling iridoi^hores ^ in their arrangement, which presumably act by reflecting the light onto the sensitive spines (Millott, 1953) (Fig. 165). It is of historical interest that the Sarasins (1887), in a much quoted paper, described similar structures in Diadema setosum, an allied species inhabiting the Indian Ocean, as being "eyes" composed of several hundred polygonal corneal facets, a vitreous-like jelly and a '' retina", but without nerve fibres. Cuf In STARFISHES (Asteroids such as the common five-rayed Asterias), although the skin is often diffusely light-sensitive, on the tip of each of the five arms a visual 1 Compare iridocytes, p. 89. Fig. 167. — The optic cushion of the Asteroid Cut, cuticle ; CT, connective tissue ; Ep, epithelium ; NN, nerve-net ; P, pigment cells. Sea-cucumber, Holothuria The sea-urchin, Diadema 186 THE EYE IN EVOLUTION organ is formed as a modified tube-foot lying on a slight elevation (the " optic cushion ") on the dorsal surface of the terminal ossicle (Fig. 166). The organ is bright red due to the presence of ^-carotene and esterified astaxanthin and consists of an aggregation of several cupulate ocelli of the simplest type covered by cuticle and lined by sensory and pig- mented cells (Plate I ; Fig. 167) (PfefiFer, 1901) ; a central lenticular body may serve to concentrate light upon the receptive elements (van Weel, 1935 ; Smith, 1937). The optical function of this organ in Asterias has been convincingly demonstrated by Hartline and his co- workers (1952) who recorded the electric impulses following stimulation by light. The terminal tube-foot appears to be olfactory in function. Berger. J. comp. Neurol. Psychol., 8, 223 Philos. Trans. B, 238, 187 (1954). (1898). Minchin. Proc. roy. Soc. B, 60, 42 (1896). Crozier. ^mer. J. P/i^sioZ., 36, 8 (1914). Pfeffer. Zool. Jb., Abt. Anat., 14, 523 Zool. Jb., Abt. Zool. Physiol., 35, 233 (1901). (1915). Prosser. J. cell. comp. Physiol., 4, 363 Dahlgren. J. Franklin Inst., 181, 377 (1934). (1916). J. comp. iVewroZ., 59, 61 (1934). Hartline, Wagner and MacNichol. Cold Sarasin, P. and F. Ergebn. naturwiss. Spr. Harb. Symp. Quant. Biol., 17, 125 Forsch.Ceylon,V^\esh&den, 1, 1 (1887). (1952). Scheer. Naturwissenschaften, 43, 501 Hertwig, O. and R. Jena. Z. Naturwiss., (1956). 11, 355 (1877). Schewiakoff. Morphol. Jb., 15, 21 (1889). Das Nervensysteyn u. die Sinnesorgane Smith. Philos. Trans. B., 227, HI (1937). d. Medusen, Leipzig (1878). von Uexkiill. Z. Biol., 40, 447 (1900). Jourdan. Les sens chez les animaux Umwelt u. Innenwelt d. Tiere, Berlin inferieurs, Paris (1889). (1909). Lehmann. Zool. Jb., Abt. Zool. Physiol., Viaud and Medioni. C. R. Soc. Biol. 39, 321 (1923). (Paris), 143, 1221 (1949). Linko. Acad. Imp. Sci. St. Petersburg, van Weel. Arch, neerl. Zool., 1, 347 Mem. Ser. 8, 10 (1900). (1935). Millott. Biol. Bull., 99, 'S29 (1950). Wellington. Nature (Lond.), 172, 1177 Nature (Lond.), 170, 325 (1952) ; 171, (1953). 973 (1953). WORMS The large group of " worms " shows a variety of visual organs as pleomorphic as the multitude of forms which constitute this loose grouping of animals, showing every variation from a unicellular eye to a relatively complex organ. In some cases the surface of the whole body seems to be sensitive to light and it has not been possible to identify specific sensory cells ; in most cases, however, specialized sensory structures occur, for the elucidation of which we are largely indebted to the classical work of Richard Hesse (1899-1908). Their presence, their number, and the degree of their differentiation vary with the animal's mode of life. This is the lowest group in the animal kingdom to show l>ilateral symmetry and the sense organs share in this general scheme distribution ; moreover, these organs are usually concen- trated 1 rds the head-end of the animal where they are of greatest biologic; lue. PLATE I The Light-sensitive Apparatus of the Starfish ^^imf>^ Fitt. 1. — Maiih ]>nsiti()ii of the eye-spot, e.s. one of which is jjresent at the tip of each of the five arms. Fig. 2. — The excised eye-spot (optic cushion) showing the o])tic cups, o.c. They have a striking red colom- due to L'-carotene and esterified astaxanthin; it is to be noted that some of the colour of the body-wall, which is also light-sensitive, is due to the same ])igments (X. ]\Iillott, Endeavour, 1957). S.O. — VOL.1 [To face 2>- 186. WORMS 187 These photoreceptors are of the most varied types and many species possess eyes of more than one variety. The neuro -sensory cells may be either apolar in type provided with an internal optic organelle, or bipolar, provided with a ciliated or striated border ^ : they may occur as single cells or in groups forming an eye of either the subepithelial or epithelial variety, in which case it may show a flat, cupulate or vesicular arrangement. Pigment is a constant association, situated within the sensory cells or in special supporting cells. If a refractive medium is present it may be formed either from the retinal or the epidermal cells, while light-refracting structures are usually cuticular in origin. As a general rule their function can only be the primitive ability to detect light, but the visual organs of some types, such as some polychaete worms, are structurally capable of some degree of localization and resolution (a directional eye) and perhaps even of visual imagery. UNSEGMEXTED WORMS The unsegmented worms may be divided into three phyla — flat- worms, ribbon-worms, and thread-worms. 1. PLATYHELMINTHES or FLAT-WORMS Constitute a gi(jup of very simply organized creatures the members of which show the progressive degeneration associated with parasitism. It is divided into 3 main classes : (a) TURBELLARiANS, freely -Swimming leaf-shaped aquatic creatures of carniv^orous habit, frequenting brackish or salt water or moist places on land ; the name is derived from the turbulence caused in the water by the beating of their cilia when they swim. They are classified accoi'ding to the arrangement of the gut — the minute marine Actf-la (without intestine), the small salt and fresh-water Rhabdocojla (rod-shaped intestine), the (mainly) marine Alloeocoela (irregular intestine), the small, flat, elongated Tricladida (3-branched intestine) found in fresh or salt water or on land (including the Planaria), and the large, leaf-like, marine Polycladida (many-branched intestine). (6) TREMATODES or FLUKES, leaf-like parasites, external or internal, found on or in all types of \'ertebrates, clinging to their hosts with suckers. Examples are the liver-fluke, Fasciola hepatica, which infests the livers of sheep and cattle, or the Schistosoma Juematobia which causes bilharziasis. (c) CESTODES or TAPE-WORMS, endoparasites, frequenting the alimentary canal of Vertebrates, including domestic animals and man, such as Taenia eckino- coccus, or T. solium. 2. NEMERTiNES or RIBBON-WORMS, ribbon- or thread-like in shape, often vividly multi-coloured, varying in size from under an inch to enormous lengths (25 metres in Linens) and provided with cilia and a remarkable retractile pro- boscis forming a tactile organ used to capture prey. Most are marine in habitat, creeping in the mud and under stones ; a few are found in fresh-water (Prostoma); some are terrestrial (Geonemertes) ; and a few live commensally with bivalves or ascidians. 3. NEMATODES, ROUND- Or THREAD-WORMS, Cylindrical in shape and often minute, which teem in the soil or in water and are often endojjarasitic in plants and animals (Ascaris, Trichinella, Ankylostoma, Filaria, etc.) ; but free-living forms occur at any rate in part of the life-cycle. 1 p. 127. Polyclad, Leptoplana Schistosoma Teen in echinococcus THE EYE IN EVOLUTION The PLATYHELMiNTHES have sense organs only of the most rudimentary type — if any. The freely-hving turbellarians (Plana- rians, etc.) are the most adequately equipped with eyes (Figs. 168 to 170). These may be merely two or four in number, in which case they lie on the dorsal aspect of the head-end associated with the tentacles near the cerebral ganglion, as in the fresh-water Rhabdocoela ; but others such as the marine Polycladida may possess several hundred. A common arrangement, well seen in the Tricladida, is that these multiple ocelli are distributed around the circumference of the body concentrated particularly at the anterior margin (Figs. 168 and 170) (Busch. 1851 ; Hyman, 1938-51). The eyes are always very elemen- FiGS. 168 TO 170. — The Eyes of Turbellarian Worms. \k s- „ M Fig. 168. — A land pla- narian, Geoplana mexi- cana. There is a row of eyes along the entire margin of the animal (after Hyman). Fig. 169.— The eyes of the pelagic Rhabdo- coele, Alaurina proli- fera. S, papillated snout ; M, mouth ; E, paired eye (after Busch). Fig. 170.— The eyes of the fresh-water pla- narian, Polycelis coro- nata. They are concen- trated at the head-end (after Hyman). Dendrocoelum tary, and lacking a dioptric apparatus are capable only of light perception although a directional appreciation may be evident (Taliaferro, 1920). The number of visual cells is said to vary between 1 and 200 (Hesse, 1896 ; Schmidt, 1902). Occasionally, as in Dendroccehim, they are of the flat epithelial type (Fig. 95). Usually they are of the subepithelial type, appearing as minute pigmented spots about 0"1 mm. in diameter and consisting of a pigmented goblet enclosing the sensory cells (Figs. 91 and 92). In these the sensory ce-lr- .T,re of the bipolar type with a striated margin facing away from tlK direction of light to form an inverted retina. When the eyes are nea ''hi^ cerebral ganglion the sensory fibres enter the latter directly ; othc -e they enter the peripheral nerve-net. WORMS 189 In some Rhabdocoela {Stenostonuni) curious hemispherical bodies consisting of refringent granules lying underneath a bowl -shaped mass have been credited with a photosensitive function ; there is no good evidence, however, for this assumption. Eyes are lacking in the cave-dwelling planarians (Kenkiidae) and in endo- parasitic Rhabdocoela.^ TREMATODES may possess simple ocelli in the larval stage (as in the liver-fluke. Fasciola hepatica), but the adults, leading an essentially parasitic existence, rarely possess sense organs. If they are present they are of the simjDlest type, usually consisting of a single cell with a striated border invested by a cup of pigment (Hesse, 1897 ; Andre, 1910 ; Faust, 1918) ; a typical example is seen in the luiicellular eye Fasciola hepatica Figs. 171 and 172. — The Eyes of Xemertine Worms. E Fig. 171. — Lineus ruber. E. eyes (after Hyman) Fig. 172. — The head of Ampkiporus angulatus. E, eyes (after Hyman). of Tristomum impiUosum. a marine Trematode jiarasitic on fishes (Fig. 87). CESTODES, in keeping with their endoparasitic life, are without sense organs. - Among the nemertines, most of which are freely-living and marine in habitat, rudimentary eyes of the same subepithelial type as occur in flat-worms are general and occasionally are very numerous (Figs. 17 1-72). They are always limited to the anterior end of the animal. Some species possess two eyes, others four or six on the prostomium ; others up to 250 eyes [Amphiporus) arranged in clusters or rows, while the number may vary in different individuals of the same species. The eyes are nearly always subepithelial in type consisting of bipolar cells terminating in a brush border enclosed within a pigment cup of epithehum (Hilton, 1921) (Fig. 93). The eyes of the terrestrial genus, 1 pp. 724, 733. "^ p. 734. Amphiporus 190 THE EYE IN EVOLUTION Nematode, Ascaris Arenirola Hcemadipsa Luinbricus Geonemertes, differ from the usual type. In these the pigmented epithehum forms a complete circle within which is a mass of refractile material ; the nuclei of the sensory cells are arranged outside the circle of pigment and their distal terminations pass through it into the central refractile mass (Schroder, 1918). In the NEMATODES, the majority of which are endoparasitic, sense organs are Hmited to papillae on the lips ; in the free-living sexual state, however, rudimentary eyes may exist, consisting of a lens-like cuticular body resting on a cup of pigmented cells (Steiner, 1916 ; Hilton, 1921 ; Schulz, 1931). SEGMENTED WOBMS (ANNELIDS) The segmented worms exhibit much diversity in habit and structure but their essential characteristics are segmentation of the body with paired appendages on each segment and a closed vascular system. Annelids are found both in marine and fresh water and on land, and in the entire phylum more than 6,500 species are known. These are divided into 4 classes, the first two of which are provided with chitinous bristles or setae for locomotion. 1. OLiGOCH^TES (with few setne), hermaphroditic creatures, essentially terrestrial in habit, typified in the common earthworm, Lumhricus terrestris, or the tiny aquatic mud-worms living in brooks or between tide-marks. 2. polycHjEtes (with many setae), essentially marine in habit ; in them the sexes are separate. Two types exist, distinguished by their habits. The more active forms (errantia) are typified in the common lob-worm, Arenicola marina, found burrowing in sandy beaches, or the freely-swimming types, such as the rag-worm. Nereis. The sedentary forms (sedentaria) are tubicolous in habit leading a sluggish life within tubes, limy, sandy or gelatinous ; as an adaptive characteristic the tentacles, gills and sensory organs are aggregated in the anterior part of the woi-m which protrudes from the tube. 3. ARCHiANNELiDS Comprise a small and anomalous class of simple marine worms with juvenile characteristics and without seta?, freely swimming or burrowing in sand and gravel. 4. HiRUDiNES or LEECHES form a highly specialized and much modified class, most of which live in fresh water in ponds or sluggish streams although a few are marine and others (the wiry land-leeches of the Far Eastern jungles, Hcemadi])sa) are terrestrial, living in inoist places. In habit they are greedily suctorial, sucking the blood of fishes, amphibians or other victims. Eyes are usually lacking in the oligoch^tes ; of those possessing visual organs, the most typical example is the earthworm, Lumhricus terrestris. Its unicellular light-sensitive organs distributed in the epithelium and aggregated around subepithelial nerves have already ])een fully described ^ (Figs. 86, 88). These visual elements are situated \N iiere they are of the greatest biological value, being concentrated at til; vo extremities, particularly the anterior. 131. WORMS 191 Thvis W. N. Hess (1925) found that in the prostomium there were some 440 light-sensitive cells in the epidermis and 700 sitviated in nearby nerve enlargements, while in subsequent segments they were much fewer. Their rela- tive numbers in corresponding sinall areas (200 x SOOti.) on the dorsal surface of the animal are as follows — in the prostomium, 18 ; 1st seginent, 10 ; 2nd segment, 5 ; 3rd segment, 3 ; 40th segment, 0 ; antepenultimate segment, 1 ; penultimate segment, 1 ; last segment, 4. The segiuental photic sensitivity varies directly with the number of receptors, and the distribution of light-sensitive elements conforms with the habits of the earthworm. ^ Among POLYCH.ETE woEMS. the burrowing lob-worm, Are^iicola marina, is not provided with visual organs although the prostomial Fig. 173. — The Head of Nereis, Showing the Four Eyes. e, eyes ; j, jaw ; p, palp ; pe, peristomium (first two segments fused) ; ph, pharynx ; pp, first ordinaiy paraijodium ;\ pr, prostomium; t, accessory teeth ; tc, tentacular cirri ; te, tentacle. (From Borradaile's Manual of Elementary Zoology ; Oxford University Press.) lobes are diffusely sensory. In contrast with the burrowing type, however, the freely-swimming marine polychaetes show a much richer development (Fig. 173). Of these, Nereis is a typical example. This worm has four prominent eyes situated on the prostomium, each of the cupulate type with a cuticle externally and a retina internally formed of well-developed sensory cells with rod-like receptor endings (Fig. 101). Other forms, such as Polyoplithalmus, have in addition to the prostomial eyes similar pairs of subepithelial organs in many segments of the body ; such eyes ^ are formed sometimes on each segment {Myxicola (esfhetica ; Eunice), and occasionally on the anal segment {Fabricia). A much more complex type of e}e of the vesicular type is found 1 p. 572. ^ These organs, usually considered to be " eyes " are said by some to be liglit- producing (p. 736) (Benham, 1896). Nereis 192 THE EYE IN EVOLUTION Branchiomma in certain pelagic polychsetes such as Alciopa and Eupolyodonfes, the intimate structure of which has already been described. ^ These worms have two eyes, sometimes facing forwards {Eupolyodontes), sometimes diverging widely (Alciopa) (Fig. 174). Each organ is provided with an elaborate retina, a lens, an accom- modative mechanism and extra-ocular muscles suggesting the potentiality for binocular vision, an equipment which seems capable of considerable visual powers approximating those of the Cephalopods.2 Little, however, is known of the habits of these worms. In the sedentary tubicolous poly- chsetes (Potamilla, Branchiomma, Dasy- chone, etc.) the ocelli are frequently grouped in masses on the branchial fila- ments to form a composite simple eye of great complexity (Brunotte, 1888 ; Andrews, 1891 ; Hesse, 1896) (Figs. 175 and 176) ; Vermilia infundi- bulum has at least 220 ocelli on the external aspect of each branchium, a total of some 11,000 eyes (Parker and Haswell, 1940). These creatures live within their tubes from out of which extend the branchial plumes bearing the filaments on each of which there is one or more such eyes (Figs. 128, 129). The curious thing, however, is that in Figs. 175 and 176. — The Complex Eyes of Tubicolous Polych^tes. e Fig. 174. — The Anterior End of THE Polych^te Wokm, Alciopa. Showing the two large eyes (after Greeff). Fig. 175. Fig. 176. The secondary filaments are seen issuing horizontally from the central axis of the branchial filament. Fig. 175, Branchiomma, showing the single complex eye, e, near the termination of the central axis. Fig. 176, Dasychone, showing the row of complex eyes (2 of which are marked e) running up and ';osvn the central axis (after Benham, Camh. Nat. Hist.). 143. Fig. 112. WORMS 193 Branchiomma, at any rate, these structures do not seem to be essential for the most characteristic responses of the worm to changes in tlie intensity of hght (Millott, 1957) ; the position is therefore somewhat anomalous. In the simple marine archiannelids, eyes of a similar type are found. In Dinophilus, for example, a minute worm found among alga^, two kidney-shaped pigmented eyes are found on the prostomium (Hilton, 1924) (Fig. 177). LEECHES (hirudinea) may be provided with visual organs of a simple type varying in number from 2 to 10 (Hesse, 1897 ; Herter, 1932) ; they are incajDable of optical imagery although highly light- sensitive, but in some species may be absent. They are found near the anterior extremity of the body and vary considerably in their morphology, but the visual cells are always of the spherical apolar type with a central optic organelle (Figs. 178-9). Fig. 177.— The rchiannelid, DlXOPUlLUS. Showing the paired ocelli, Oc (after Sheldon- Harmer). In Branchellion these organs are unicellular; in Piscicola they consist of 12 cells arranged in a row surrounded by pigment. In Hcemopis both unicellular and multicellular ocelli are found (Fig. 179). In the common medicinal leech, Hirudo medictnalis, there are segmental papilhe with a sensory function on the middle ring of each of the 26 segments. Although all the sense organs are serially homologous the pairs on the dorsal surface of the first five segments are purely visual, constituting ten " eyes " (Fig. 90), provided with a rich nerve supply to the cerebral ganglia. At the other extremity the Branchellion Hirudo Figs. 178 and 179. — The Eyes of Leeches. Fig. 178. — The head end of the medicinal leech, Hirudo niedicinalis. The dorsal aspect. The body is divided into segments, each of which contains 5 rings (annulae). In the middle ring of each segment the segmental papillte have a sensory function. The first 7 (and the last 3) segments have less than the normal number of rings, and the first 5 show two paired eyes as larger black spots. El to Eg, serially homologous with the sensory papillae (see Figs. 89-90) (after Parker and Haswell). S.O. VOL. I. W^^ "..7.J-.i_ X--^'y^^^ Fig. 190. — The Common Scallop, Pectes. The pallial ocelli, Oc, are seen in a single row i-ound the margin of the mantle. For section of the eye, see Fig. 123 (after Pelseneer). pigmented cells as occurs in the j^earl-oyster, Avicula, or the edible mussel, Mytilus. More usually they are replaced by ocelli located in situations where they are of greater biological value such as the siphons, the tentacles or the mantle (Fig. 190). Thus the ocelli are found on the inner surface of the siphons in clams which habitually lie buried in the sand or mud (Mya) or bore into soft rocks (Pholas) (Light, 1930) ; as they lie buried these molluscs extend the siphon to the surface to feed and at daybreak or whenever the illumination increases the siphon is withdrawn (Wenrich, 1916 ; Hecht, 1919-20 ; Pieron, 1925 ; Folger, 1927 ; and others). It will be remembered that these visual organs are of the most simple type resembling those of the earthworm, being merely single cells of the apolar type with a refractive organelle in the cell-body richly supplied with nerves.- In the cockle, Cardium,, small ocelli are situated at the tips of the tentacles, about 100 in number, which are arranged around the siphonal apertvires ; the eye is of a simple cupulate form, the cuj^-shaped retinal cells resting on a layer of double pigmented cells underneath a large ectodermal cell^iJar lens and cornea (Kishinouye, 1894). As in the pallial eyes of Pecten, the !ct ina is inverted. Pecten 1 p. 323. p. 131. MOLLUSCA 201 Most bivalves, however, have numerovis oceUi arranged Hke a coronet around the margin of the mantle (pallial eyes) ; these may be numbered in hundreds and are probably to be looked upon as modified tentacles. In some foi-ms, such as Lima, they are very primitive. This bivalve is provided with 30 simple cup-shaped depressions, 0-3 mm. in diameter, lined with sensory and pigmented cells forming primitive cu2:)ulate eyes ; in others such as the fresh- water mussel, Anodonta, eyes are completely absent. Most of these types are relatively shiggish and quiescent, but in actively swimming forms the eyes may be more elaborate. This development is well exemplified in svich bivalves as the comnion scallop, Pecten, and Spondylus, both of which possess eyes unique among IMolluscs. The pallial eyes are arranged in a single row around the edge of the mantle ; when they are exposed as the shell gapes they shine as brilliant emerald green or purple spots, 0-6 to 0-8 mm. in diameter ; 28 to 46 have been counted in the upper half of the mantle, 15 to 36 in the lower, and each is borne on a con- tractile pedicle (Fig. 190). These are of remarkable complexity with a well-formed inverted retina which appears to be much more elaborate than the visual demands of the shell-fish would seem to warrant (Fig. 123). Each is comiected by means of its optic nerve with a large circumpallial nerve and so with the branchial ganglion.^ An anomalous occurrence in certain lamellibranch molluscs (the Noah's-ark shell. Area ; Pectunculus), is that of unicellular ocelli grouped together in a spherical mass constituting an aggiegate eye which bears a superficial resemblance to a compound eye - (Carriere, 1885 ; Patten, 1886 : Hesse, 1900). Pearly Nautilus Fig. 191. — The Nautilus, pompilius. The animal is seen in section. Above is the spiral shell. E, the eye, which opens to the exterior ; Si, siphon ; T, tentacles (after Owen). The CEPHALOPODS (cuttlefish, etc.) usually exhibit the most elaborate visual organs found among Molluscs, a characteristic understandable in view of their active be- haviour and carnivorous habits ; only one species living at abyssal ocean depths is knoAMi to lack eyes, Cirrofhauma murrayi? They are the most specialized of the molluscs and i:)resent considerable diversities of type, but most of them are freely SAvimming and they all have a \vell-develoj)ed head furnished with numerous "arms" bearing tentacles or suckers and provided with eyes and other sensory structures. In the pearly nautilus of the seas of the Far East, the sole survivor of the primitive and almost extinct tetrabranchiate Cephaloi^ods which were largely Palaeozoic in distribution, the eye retains its ancestral simplicity and consists merely of an epithelial depression with a tiny aperture 2 mm. in diameter (Figs. 100 and 191) ; it is situated on a raised flat peduncle which is also provided witli two " ocular tentacles "', probably olfactory in function. In the more recent and voraciously carnivorous dibranchiate Cephalopods, however, such as the common cuttlefish, Sepia, the Ayiodonta Spondylus Sepia p. 1.51. J23. 202 THE EYE IN EVOLUTION squid, Loligo, and the octopus, the two eyes are large and prominent (Figs. 192-3). They are situated conspicuously on either side of the head behind the main body of tentacles, protected in part by the cartilage surrounding the brain and in part by cartilages in their own Fig. 192. — Octopus vulgaris (J. Z. Young). walls, and provided with rudimentary lids and a set of 4 extra-ocular muscles which confer a wide range of movement on the globe (Hesse, 1908 ; Tompsett, 1939) (Figs. 113 and 114). The complex structure of these organs has already been described, ^ and although they rival the eyes of Vertebrates in their morphology, they are simple in type, derived from the epithelium. The close resemblance of the eyes of these molluscs to the cerebral " camera " eyes of Vertebrates is a striking examjDle of convergent evolution whereby Nature achieves comparable results by travelling along entirely different routes. The nervous connections are promi- nent ; in the posterior wall of each eye is a large optic ganglion from which the thick optic lobes lead directly to the closely associated cerebral ganglion ^ (Fig. 698). There is a well- developed olfactory sac behind each eye as well as two statocysts and organs of general sensa- tion, but it would seem that vision plays a dominant part in the behaviour of the animal.^ The Common Loligo vul- the two large f^yes, one on the head in). 143. 575. 2 p. 5: MOLLUSCA 203 Anomalous types of eyes are seen among Cephalopods found at great ocean depths (Chun, 1903). Stalked eyes comparable to those found in some deep-sea fishes, are exemplified in Bathothauma (Fig. 194) and Srindalops (Fig. 195) ; both of these live at great depths in the South Atlantic and the eyes of the latter are unic£ue in that they point obliquely downwards, a curious configvu'ation said to be explained by the fact that the squid swims with its body slanting upwards. Figs. 19-1 to 196. — The Eyes of Dkep-sea Cephalopods. Fig. 19.5. Fig. 194. Fig. 196. Fig. 194. — The deep-sea squid, Bathothauma. There are luminous organs beside the eyes which are perched on the end of stalks. Found at a depth of 3,000 m. (from the Valdtvia Reports). Fig. 19.5. — The deep-sea squid, Sandalops melancholicus. The stalked eyes are unique in that they point obliquely downwards, possibly because the animal swims with its body slanting upward (from the Vahlivia^ Reports). Fig. 196. — The pelagic octopus, Amphitretus. The tubular eyes point upwards and the whole body, including the eyes, is covered with a delicate gelatinous covering (from the Valdivia Reports). Another curious arrangement is seen in Amphitretus (Fig. 196) found in the Indian and Pacific oceans. The eyes of this octopod resemble the tubular organs of some deep-sea fishes, i pointing directly upM^ards and enclosed, as is the entire body of the animal, in a delicate and transparent gelatinous covering. Boulet. C. B. Soc. Biol. (Paris), 148, I486 (1954). Carriere. Die Sehorgane der Ticre, Miin- chen(1885). Arch, niikr. Anat., 33, 378 (1889). Chun. Verhdl. dtsrh. Zool. Oes., 13, 67 (1903). Crozier. J. gen. Physiol.. 2, 627 (1920). Folger. Anat. Rec, 34, 1 b5 (1927). Galati-Mosella. Motiit. Zool. ital., 26, 75 (1915). Hecht. J. gen. Phi/xioL, 1, 545, 657 (1919) ; 2, 337 (1920). v. Hess and Gerwerzliagen. ^4rc/(. vergl. Ophthal.,^, 300 (1914). He.sse, R. Z. ^ris.<.■. Zool.. 68, 379 (1900) ; 70, 347 (1901) ; 72, 565, 656 (1902). Das Sehen der niederen Tiere, Jena (1908). ' p. Kishinouye. J. Coll. Scl. Imp. Univ. Japan. 4, 55 (1891) ; 6, 279 (1894). Light. J. Morphol. Phi/siol.. 49, 1 (1930). Moseley. Ann. Mag. not. Hist., 14, 141 (1884). Mtiller, J. Ann. Sci. nat., 22, 5 (1831). Nowikoff. Z. wiss. Zool., 88, 153 (1907). Patten. Mitt. zool. Stat. Neapel, 6, 546, 568, 605 (1886). Pieron. C. R. Soc. Biol. (Paris), 93, 1235 (1925). Plate. Zool. Jb., Suppl. 4, 1 (1899). Prince. Te.ras J. Biol. Med., 13, 323 (1955). Tompsett. Liverpool marine biol. Comm. Mem., 32, 1 (1939). Wenrich. J. anim. Behav., 6, 297 (1916). Willem. Arch. Biol.. Gand. 12, 57 (1892). 322. 204 THE EYE IN EVOLUTION ARTHROPODA ARTHROPODS embrace more than three-quarters of the known species of animals, and in view of their number and variety and the diversity of their habits, it is not surprising that an extraordinary variation occurs in their visual organs, while the intense and purposive activity of many of them accounts for the complexity and efficiency of their eyes. Arthropods are characterized by their bilateral symmetry, their cegmental structure with jointed appendages, their chitinous cuticle, a distinct head where the sense organs are aggregated, and a nervous system consisting of a dorsal brain-ganglion connected by a ring round the gullet with a double chain of ventral ganglia. From the ocular point of view, although simple eyes often of quite a rudi- mentary type are frequent, and may indeed be the sole visual organs (as in Arachnids), the characteristic feature of the phylum is the presence of compound eyes of elaborate structure and frequently with highly developed functional abilities. The Arthropods may conveniently be divided into five sub-phyla : (1) the primitive worm-like onychophora, unique in having a soft, velvety skin, and provided with a separate head, one pair of antennae and 20 legs all alike ; (2) the CRUSTACEANS, comprising some 25,000 species, with the head fused with the thorax, 2 pairs of antennae and at least 5 dissimilar pairs of legs ; (3) the MYRiAPODS (centipedes, millipedes, etc.), of some 2,000 species, with a distinct head, one pair of antennae and numerous legs all alike ; (4) the ARACHNIDS, of some 36,000 species, having 2 body -segments with a fused cephalothorax, without antennae or wings, and 4 pairs of legs ; (5) the INSECTS, of which more than 577,000 species have now been scientifically described and probably several times as many await investigation, with a body divided sharply into 3 segments, head, thorax and abdomen, bear- ing one pair of antennae, 3 pairs of legs and (usually) one or two pairs of wings in the adult. ^ Fig. 197. — The Onychophore, Peripatus. Note the two simple eyes on top of the head at the base of the anten- nae (Thomson's Zoologij, James Ritchie ; Oxford Univer.^ity Press). ONYCHOPHORA The most primitive class of Arthropods, the ONYCHOPHORA {Peripatus and its allies), inhabiting the forests of the Southern Hemisphere, represent an archaic type, differing widely from other members of the phylum. Seeking out damj) places under leaves ^ In oue acre of farm-land in England it has been estimated that there are from 700,000,or^:; to 800,000,000 Insects and as many Arachnids. They would usurp Man's do. .11 it ion of the earth were their numbers not kept in check by voracious predators ^ parasites of their own kind. ARTHROPODA 205 and in rotting wood, they are shy and nocturnal in habit with a marked dishke of hght. They are beautiful, velvety, caterpillar-like creatures with paired eyes set like diamonds (0- 2 to 0- 3 mm. ) on the side of the head behind the two sensitive antenna?, looking upwards and outwards, not forwards (Fig. 197) ; the eyes, like those of marine Polychsetes, are of Figs. 198 TO 200. — The Eyes of the Large Crustaceans (Decapods) (Specimens from Natural History Museum, London). Fig. 199. Fig. 198. Fig. 200. Fig. 198. — The common shrimp, Crangon vulgaris. The short eye-stalks bearing the compound eyes lie in sockets in the carapace. Fig. 199. — The fiddler crab, Gelasimus arcuatus. There are two com- pound eyes, C, each standing out prominently on a muscular eye-stalk and protruding on either side of the median rostrum. The left claw is repi-esented by a small stump ; the huge right claw gives the animal its name. Fig. 200. — The racing crab, Ocyilpoda ippens. Two j^rominent elongated compound ejes, C, are set on eye-stalks, in sockets on the carapace. 206 THE EYE IN EVOLUTION the simple type, cupulate in form with a corneal lens formed by the cuticle and hypodermal cells (Fig. 103). Eyes so simple as this serve merely as a means of orientation away from light, and two cave- dwelling species are blind ^ (Dakin, 1921). CRUSTACEA The CRUSTACEANS (lobsters, crabs, shrimps, water-fleas, barnacles, etc.) with few exceptions (land-crabs, wood-lice, sand-hoppers) are aquatic in habit and in most the eyes are prominent ; some pelagic forms are transparent except for the eyes which are highly coloured or phosphorescent. Compound eyes are usually present, occasionally supplemented by eyes of the simple type, but in sessile or parasitic forms the visual organs may be vestigial or lacking. Most forms Q Fig. 201. — The Woodlouse, Sph.sroma lanceolata. The compound eyes, C, are sessile, lying on the extreme lateral aspects of the head segment (specimen from Natural History Museum, London). Homams Phronima commence life as a nauplius larva with an oval body, three pairs of limbs and a single eye in the middle of the head. Of the larger forms (the sub-class malacostraca) the Decapods (lobsters, shrimps, prawns, crabs) have the most elaborate eyes ; of these the common lobster, Homarus vulgaris, may be taken as repre- sentative. It possesses two typical compound eyes, each with a multi- tude of ommatidia, associated with the procephalic lobes of the cerebral ganglion. They stand out prominently on muscular eye-stalks to protrude on either side of the median rostrum and are capable of some degree of movement (Fig. 198). In crabs a similar pair of compound eyes with relatively few but large ommatidia are set on eye-stalks in sockets in the carapace (Figs. 199-200). The fact that the eye-stalks L. ^Hi in the crab and in the crayfish exhibit optomotor reactions as when tJir- animal turns or is confronted by a black and white striped rotating dr^ ', indicates that their movements are optically determined 1 p. 724. ARTHROPODA 207 (v. Buddenbrock ei ah. 1954 ; Dijkgraaf, 1956). One group, the Eryonidea, confined to the deep seas, are blind, the eyes being reduced to stalks only. In other species the eyes are sessile, both in terrestrial Isopods (such as woodlice, Fig. 201) and in pelagic Amphipods : among the latter in the smaller forms the eyes may be minute {CapreUa, Fig. 202), while in the larger forms they may assume enormous dimensions (the " wondrous-eyed hopper," Thaumatojis magna. Fig. 203). Sedentary types such as Asellus, an Isopod which lives in holes, are completely blind. Fig. 202. — The Amphipod, Caprella LjyEJItl.s. Two ocelli are seen on the dorsal surface of the head. Fig. 203. — The " Wondrous-eyed Hopper," Thaumatops magxa. The largest known hyperiid Crusta- cean, found at a depth of 2,500 in., with enormous compound eyes (to the right) (f natural size) (after Brehm). Euphausiid Crustacean Asellus The smaller Crustaceans (branchiopods, cojDepods, ostracods, cirripedes) include a vast number of types in which the active swimming forms are provided with eyes, while in most sessile and j)arasitic forms the organs become degenerate. They comprise four diverse and little related orders : (a) BKANCHiOPODS — protected by a shell and provided with 4 pairs of leaf- like swimming feet. They comprise tw'O groups : (1) the phvllopoda such as the brine-shrimp, Artemia, which can survive even in Salt Lake, and the large fresh-water Apus, of world-wide distribution, and (2) the laterally compressed minute water-fleas (cladocera), Daphnia, Polyphemus and Leptodora, so abund- ant in fresh water. (6) OSTRACODS — small laterally compressed creatures with a bivalve shell and indistinct segmentation, breeding parthenogenetically. Typical examples are the fresh-water Cypris and the salt-water Cypridina. (c) COPEPODS — elongated segmented creatures without a protective shell. Typical examples are the beautiful fresh-water Cyclops and the salt-water Calanus. Copepods occur in vast numbers in the seas and constitute the most Artemia Leptodora Calanus 208 THE EYE IN EVOLUTION Nauplius larva abundant animal constituent of the plankton. The group also contains some parasites, as the common fish-louse, Caligus. {d) ciKRiPEDE.i — with an indistinctly segmented body and usually provided with a calcareous shell. They have a complex life-history. They are born as actively swimming nauplius larvae, develop into a pupal cypris-like stage, again swimming freely with appendages, but in the adult condition lead an entirely sessile or parasitic life. Typical examples are the barnacle, Lepas, which attaches itself to the bottoms of ships or floating logs, the acorn-shell, Balanus, which Figs. 204 to 206. — The Eyes of Small Crustaceans (Specimens from Natural History Museum, London). c X^^ i^ Fig. 204. Fig. 204. — The dorsal surface of a Branchiopod, Triops [Apus) cancri- formis. In the anterior region are two compound eyes, C, and behind them a median eye of the composite simple type, S. Fig. 205. — An Ostracod, Cypria ophthalmica. The single deeply jjigmented eye, E, is seen shining through the semi-transparent shell. Fig. 206. — The water-flea, Daphnia. Prominently in the head region (at the junction of the arrows) is the compound eye, ajDijearing as a mass of pigment with little facets romid it. Behind and underneath lies the minute composite median ej^e (see also Fig. 145). j encrusts the rocks between tidal marks in enormous numbers, and Sacculina, ■.■!ie of the most degenerate of parasites which becomes an endoparasite in the i.-' •' anen of crabs. of rhe characteristic ociilar feature of the whole group is the presence uedian unpaired eye ; it is sometimes unique, as in Cyclops^ ARTHROPODA 209 sometimes associated with a single compound eye, as in Daphnia, sometimes with paired lateral eyes which may be either simple, as in PonteUopsis, or comp>ound in type, as in the Phyllopod, Apus (Fig. 204). In Apus the median eye is really a paired organ but the two are so closely situated that they appear on examination to be a single spot. The median e^-e of these small Crustaceans is situated either dorsal or ventral to the cervical ganglion and is of the composite simple type ^ ; it is comjDosed of the fusion of a number of constituent ocelli (usually 3). Such a median eye is present in most of the Branchiopods and Ostracods, only occasionally degenerating when the compound eyes are particularly well developed {Polyphemus, Leptodora). The ocular arrangements in these actively swimming small Crustaceans is therefore very varied. The eyes of the water-flea, Daphnia, may be taken as representative of the Branchiopods and Ostracods. There is a single compound eye in the mid-line composed of 22 relatively rudimentary ommatidia (Fig. 206). Behind and below this, buried in the central nervous system, is the small composite ocellus (Figs. 131 and 145). It is interesting that the compound eye is actively motile, being kept in a state of continual vibration by 4 muscles somewhat resembling in their arrangement the rectus muscles of vertebrates (Rabl, 1901 ; Hess, 1912). It would seem that the small composite ocellus is of little functional value. The phototactic responses exhibited by the animal depend entirely upon the more elaborate compound eye ; when this has been removed the phototactic responses fail although the more primitive generalized sensitivity to light persists (Schulz, 1928 ; Harris and ^lason, 1956). The eyes of some of the actively swimming Copepods take on another form. In the female PonteUopsis regalis, there are two very small dorsal ocelli sym- metrically placed and a large unpaired median eye situated fronto -vent rally underneath the rostrum ; it has a large cuticular lens and 6 retinal cells arranged in an inverted position in two groups of 3, forming an intermediate step between a simple eye and an ommatidiura (Vaissiere, 1954-55). The elongated, actively motile eyes of Copilia are of the same general structure with a retinule of 3 sensory cells (Fig. 139) (Grenacher, 1880-95 ; Exner, 1891). This animal has two such eyes facing forwards and widely separated ; in Sapphirina they are close together ; and in Corycceus so close that the lenses ai-e fused in the mid-line. Polyphemus Copilia Balanus In sessile forms eyes are usually present in the actively swimming nauplius stage ; thus in the acorn-shell, Balanus. there is initially a median unpaired eye but after several moults in the pupal stage two lateral composite eyes are acquired. In adult life, however, these become vestigial, as also does the unpaired eye of the ship-barnacle, Lepas (Fales, 1928). In some parasitic forms such as the fish-louse, Caligus, both median (sim^^le) and lateral (composite) eyes are also present, but in degenerate types such as SaccuJina eyes and other sense organs are lost. 1 p. 152. Lepas S.O. —VOL. I. 210 THE EYE IN EVOLUTION MYRIAPODA The MYEiAPODS (the quick-moving, carnivorous solitary centipedes or Chilopoda^ some with more, some with less than 100 legs, and the slow-moving vegetarian, gregarious millipedes or Diplopoda) are characterized by the possession of two groups of ocelli forming aggregate eyes on either side of the head so closely packed together as to suggest a compound eye (Figs. 207 to 210); so close are they in the Chilopod, Scutigera, that they form a pair of true compound eyes (Grenacher, Figs. 207 to 210. — The Aggreg.a.te Eyes or Myriapods (Specimens from Natural History Museum, London). Fig. 208. Fig. 209. Fig. 210. Figs. 207 and 209. — The centipede, ScoJopendra morsitans from India. The jToup of 4 ocelli, E, are situated on either side of the head. ■ ':s. 208 AND 210. — A iSpirostreptid millipede from the Seychelles. Thi .iip of ocelli forming an aggregate eye, E, is seen on either side above the a , iinae. Fig. 210 shows the close resemblance to a true compound eye. ARTHROPODA 211 1880; Graber, 1880 ; Caesar, 1913 ; Const ant ineanu, 1930). In some types, such as Pauropus, which live in moist debris in the woods and forests, eyes are lacking. ARACHNIDA The ARACHNIDS form a large and loosely associated group which includes scorpions, king-crabs, spiders, pseudo-scorpions, whip-tailed scorpions, harvest-men, jerrymanders, mites and ticks. With the single exception of the king-crab they do not possess conii^ound eyes Fig. 211. — The Kikg-crab, Limvlus polypbeml's. A .simple ej'e, S, is seen as a dark spot situated on either side of the median spine. The two compound eyes, C, are situated on the external aspect of each of the first lateral spines (specimen from Natural Historj^ Museum, London). but all are provided with ocelli sometimes of considerable size and complexity. SCORPIONS (scorpionidea), venomous animals up to 8 in. in length with a long stinging tail, are restricted to warm countries ; in habit they are essentially solitary and nocturnal, being active during the night and spending the day lurkmg under stones or in crevices. They are provided with a pair of large median eyes situated about the middle of the cephalothorax, and 2 to 6 pairs of lateral ocelli placed on its antero-lateral margins, the more anterior being simpler in structure than the posterior.^ The lateral eyes are simple ocelli in which the 1 p. 141. Scorpion 212 THE EYE IN EVOLUTION borders of the visual cells unite with their neighbours to form rhabdomes (Fig. 109) ; the median eyes are also of the simple type with the sensory cells arranged in groups each centred on a rhabdome. These cells, however, are peculiar in that they are doubled upon themselves to form a semi-inverted retina ^ (compare Fig. 127). ^ The KING-CRABS (xiphosuea), a very ancient type dating to the Silurian, w^hich live in shallow water on the sandy shores of North America {Limulus) or Asia, have two large lateral compound eyes and two median ocelli (Fig. 211). The compound eye is of a unique and elementary type ^ (Fig. 143) ; it is not faceted but is covered by a chitinous thickening of the cuticle which sends projections inwards as Ki( 'I'll i: .1 I Mi'iN(. Si'i 1 'i:i!, /'/ / A //■ SIM'ATL'f!. From the Dutch East Indies. The 2 large and 6 small simple eyes are seen surrounding the anterior and lateral aspects of the carapace (specimen from Natural History Museum, London). conical papillse over each ommatidium to form a corneal lens. The small median eyes are of the simple type wherein the sensory cells are associated with rhabdomes (Fig. 142). In addition, a third pair of ventral eyes is present in the larva on either side of the frontal organ of the hypostoma. an olfactory organ ; in the adult these eyes become degenerate but it is possible that they may participate in the olfactory function (Patten, 1893 ; Hanstrom, 1926). 2 F ' details, see J. Miiller (1826), Lankester and Bourne (1883), Parker (1887), Petrun! -li (1907), Police (1908), Scheuring (1913-14). Biitschli (1921), Versluys and Deu: 1923). "p. ARTHROPOD A 213 SPIDERS (araneida) are of widespread distribution and, although comprising some 14,000 species, are conveniently divided according to their habits into two types, the relatively sedentary " web-spinners " and the more active " wanderers " which hunt their prey ; all, how- ever, sjiin silk, either as a web, or for snaring or tying up their victims, for protection of their cocoons or for making bridges for travelling. In both types on the cephalothorax there are G or more usually 8 simple eyes arranged in two or three rows (Fig. 212) ; these have received a c«j:>'' ^'^rable amount of study. ^ The arrangement of these ocelli varies remarkably (Figs. 213 to 216). Among the web-spinners the ocelli are rudimentary and their effective range is short. The common house Figs. 213 to 216. — The Arrangement of the Ocelli in Different Species of Spiders. Fig. 213. — The ocelli of tlu* comtnon house spider, Te'jcu'irio doinestica. Fic;. 214. — The ocelli of the common garden spider, Araueus dldilcmatus. Y\Q. 21.5. — The ocelli of the wolf FiG. 216. — The ocelli of the jumping spider, spider, Li/ro.sd lujricoht. Salticus scenicu.s. 1 For details, see Hentschel (1899), Widmann (1908), Petrunkevitch (1911), Scheuring (1914), Versluys and Demoll (1923), Savory (1928), Homanu (1928-53), Millot (1949). 214 THE EYE IN EVOLUTION Tegenaria Aratieus Salticus Whip-scorpiou spider, Tegenaria domestica, has two rows of 4 ocelli, those of the anterior row being slightly smaller than those of the posterior (Fig. 213); the common garden spider, Araneus diadematus, has 4 median and 4 small lateral eyes (Fig. 214). The more active hunting species which construct no web have larger eyes ; thus the wolf-spider, Lycosa, has an anterior row of 4 small ocelli, two large posterior median and two smaller posterior lateral ocelli (Fig. 215) ; while the jumping- spider, Salticus, with a visual capacity more fully developed than the wolf-spider, has an anterior row of two large and two smaller ocelli on the front of its square-shaped cephalothorax, and two very small posterior median and two posterior lateral ocelli on the top (Fig. 216). With all its variations the general plan is thus consistent ; the anterior median eyes (the two central eyes in the front row) have a verted retina, the remainder are inverted provided with a crystalline tapetum ^ and since these latter glow in the dark the former are some- times called " diurnal eyes." The nerve-fibres from the two anterior median eyes travel — with a partial decussation at a chiasma — to the ganglion of the first cephalic segment, from the remaining eyes to that of the second (Figs. 107, 126). It is interesting that the anterior median eyes of spiders are equipped with muscles attached to their posterior aspect rendering them motile so that they can increase their visual field ; thus web-spiders have one muscle, Lycosids two, and Salticids six. These are absent in the lateral and posterior median eyes. Curious anomalies to this general arrangement exist, but they are rare ; thvis in the female of a spider found in France, Walckenaera acuminata, the eyes are arranged on a dumpy tubercle on the cephalothorax, while in the inale they are perched on a long stalk-like periscope, 4 on the tip and 4 half-way down (Millot, 1949). It is interesting that among spiders the lens, which is part of the outside covering of the animal, is cast at the time of moulting and thtis it would appear that the spider may be ren-dered temporarily blind. PSEUDO-SCORPIONS (pseudoscorpionidea), minute animals resem- bling miniature scorpions but without the long tail and sting, found burrowing in books or under stones, the bark of trees and the wing- covers of insects, are provided with two pairs of simple eyes (when they exist) on either side of the cephalothorax ; the^e are typically equipped with an inverted retina and a tapetum (Scheuring, 1913) (Fig. 217). w^HiP-TAiLED SCORPIONS (PEDiPALPi). The eycs of this order are not well known (Scheuring, 1913 ; Versluys and Demoll, 1923 ; Millot, H'49). They are entirely absent in some species ; in others there are two median eyes only ; but the typical arrangement consists of two median (principal) eyes and two groups of 3 lateral eyes. ' Except Salticus, the eyes of which lack a tapetum and are therefore " diurnal ". See fr '-■ p. 1.50. ARTHROPODA 215 The median eyes are of the cupulate type with a semi-inverted retina the cells of which are doubled upon themselves ^ (Fig. 127). The lateral eyes have an inverted retina with a tapetum (Fig. 124). Fig. 217. — The Pseudoscorpion, Carffosius ischsocbules. Showing two simple eyes, S, on either side (specimen from Natural History IMuseum ) . HARVESTMEN (PHALAXGIDA ; OPILIONES), minute spider-like Arachnids with extremely long legs, which avoid the glare of daylight, have two simple ocelli mounted one on either side of an oculiferous tubercle (ocularium) (Fig. 218). It would seem that with its laterally directed eyes the animal has no frontal vision. Each ocellus is a simple Harvestman As^. *** Fig. 218. — The Eye of the Harvestman, Megabusus diadem a. The smiple eye is seen on a siDecial oculiferous tubercle (specimen from Natural History Museum). cupulate eye with a large cuticular lens and a simple row of visual cells from which the fibres emerge in several branches to form the optic nerve (Purcell, 1894). ^ p. 1.50. 216 THE EYE IN EVOLUTION Jerrymander JEBRYMANDERS (soLiFUG^) — active, pugiiacious, non-venomous, nocturnal creatures found in warm countries — possess a pair of median (principal) eyes situated on a small tubercle and one or two pairs of lateral eyes usually rudimentary, difficult to see and probably function- less. Both types are simple cupulate ocelli with direct (verted) retinse (Scheuring, 1913; Demoll, 1917). MITES and TICKS (acarina). mites are minute Arachnids of which over 20,000 species are known, found almost universally in the earth or in water, salt and fresh, often of parasitic habit on or within animals (including man) and plants whether alive or decaying after death : well-known human j^arasites are SarcojJtes scabiei (the itch-mite) causing scabies, and Dernodex foUiculorum found in the hair follicles ; the harvest-mite (chigger) is a virulent pest to both man and animals (particularly rodents), while others infest insects (Isle of Wight bee disease) and others plants (gall mites, red spiders, etc.). Many, such as SarcojJtes are without eyes (Fig. 219) ; others, such as the Prostigmata and the Hydracarina (fresh-water mites) are pro- vided with 2, 4 or 6 ocelli on the front and lateral aspects of the head depending on the species, the individual organs being sometimes fused (Fig. 220 and 221) (Lang, 1905). Each possesses a convex lens often difficult to distinguish from the surround- ing skin. TICKS (ixoDiDEs) are larger than mites and are frequently of biological importance as causing disease (tick-fevers) in man ^ and animals. 2 Most types are without eyes, but such species may have thin transparent areas on the dorsal surface which perhaps respond to differences in the intensity of light. When visual organs are present they are extremely rudimentary, being minute ocelli mounted curiously on the animal's shoulder (Fig. 222). Figs. 220 and 221. — The Eyes of Fresh-water Mites (Hydracarina). Fig. 219. -The Mite, Sarcoptes SCABIEI. (Female) ( X 125) (Sutton and Sutton, Hh. o/ Dis. of the Skin, Mosby). Fig. 220. — The 4 separate ocelli of Limnesia. Fig. 221. — Hijgrobates, showing fusion of the anterior and posterior ocelli (after P. Lang). ^ Texas fever. Rocky Mountain spotted fever, etc. 2 Red -water fever in cattle, heart -water in sheep, etc. ARTHROPODA 217 SEA-SPIDERS (PYCNOGONiDA ; pantopoda). marine species related to the Arachnids, inhabit the shores or the depths of the seas, Hving on seaweed, hydroids and sponges. They are provided with 4 primitive oceUi perched in two pairs on an ocuHferovis tubercle on the cephalothorax ; as we have already noted, the retinse are of a jieculiar and characteristic inverted type ^ (Morgan, 1891 ; Korschelt and Heider, 1893 ; Sokolow. 1911 ; Schlottke. 1933) (Fig. 125). Fig. 222. — The Tick, Amblfomma pompo.^vm. The two simple eyes, S, lie well posteriorly on the shoulder of the animal (specimen from Xatural History Museum). Pj'cnogonid IXSECTA INSECTS form the largest class of Arthropods and their multitude of types is subdivided with reference to their possession of wings ; it is interesting that the complexity of their eyes varies directly with this characteristic, an association only natural in view of the demands made upon vision by a high degree of mobility. (1) Sub-class APTERYGOTA (d, privative ; -nrepv^ a wing), wingle.gs forms, in which through a series of moults the adult differs little from the newly hatched insect except in size. They are the most primitive of insects, some species being marine, and when eyes are present they are simple in type. THYSAXURA — bristle-tails, of wide distribution in damp soil, son"ie living between tide-marks or under stones or bark ; others (silver-fish) in bread-bins or books. Closely related are the eye-less diplura. PROTURA — ininute creatures (2 mm.) living in moist soils vmder stones and bark, without wings, antennae or eyes of anj^ kind. COLLEMBOLA — .sjiringtails, living under stones and leaves ; one species lives between tide-marks. (2) Sub-class pterygota, provided with wings which, however, may be secondarily lost through highly evolved specialization. The sub-class is divided 1 p. 150. 218 THE EYE IN EVOLUTION TYPICAL INSECTS : I (Draivn not to scale but approxitnately to a standard size.) THYSANURA APTERYGOTA PROTURA COLLEMBOLA Silver-fish Acerentonion EXOPTERYGOTA ORTHOPTERA Springtail DERMAPTERA Cockroach Grasshopper Stick-insect Earwig PLECOPTERA ISOPTERA PSOCOPTERA ANOPLURA Stone-fly Termite Book-louse Pediculus EPHEMEROPTERA THYSANOPTERA HEMIPTERA Thrip Bed-bug ARTHROPODA 219 TYPICAL INSECTS : II (Drcuun not to scale but approximately to a standard size.) EXDOPTERYGOTA NEUROPTEHA TRICHOPTERA LEPIDOPTERA Lacewing Caddis-fly Butterfly Moth COLEOPTERA ^ky A. Colorado beetle, Leptinotarsa Burying beetle, Necrophorus Rose-chafer, Cetonia Fire-fly, Photinus HYMENOPTERA Bee, Bombus Wasp, Vesjm Ant APHANIPTERA Blue-bottle, CalUphora Gad-fly, Tabanus Bee-fly, Bombiiliiis Flea, Pulex irritans 220 THE EYE IN EVOLUTION into two, depending on whether their wings are developed externally (Exoptery- gota) or internally (Endopterygota) ; in the latter the wings become evident only in the adult (imago) stage. (a) EXOPTERYGOTA, insects which undergo a series of moults marked by the gradual development of wings. The more important orders are : — • ORTHOPTERA — cockroaches, locusts, grasshoppers, crickets, stick- insects, praying mantis. DERMAPTERA — earwigs. PLECOPTERA — stone-flies, a small and little known order, the aquatic larvte being found beneath the stones of mountain streams, and the slow-flying adults having a very short life. ISOPTERA — termites living under grovmd without eyes. EMBIOPTERA — a few species of insignificant tropical insects. ZORAPTERA — a few species of minute insects resembling termites. psocoPTERA — small plump, book-lice (winged or wingless). ANOPLURA — biting or sucking lice, wingless, parasitic on man and animals and frequently disease-producing {Pediculus, Phthirus, etc.). EPHEMEROPTERA — mayflies, the aquatic larva3 living up to 3 years, the delicate adult a few hours. ODONATA — brilliantly colovired dragonflies and demoiselle flies with aquatic larvae, the former unusually active, swift-flying and voracious, the latter more delicate. THYSANOPTERA — the minute thrips, vegetarian in habit, living on flowers, leaves and decayed vegetation. HEMiPTERA — bugs with a specially developed proboscis (rostrum) adapted for piercing and sucking, many of them beautiful and slender despite their name : land bugs including the bed-bug, water bugs varying from the giant flsh-killer or the water-scorpion to the water boatman (Notonecta), the cicadas, the frog-hoppers, tree-hoppers, leaf-hoppers, the aphids (or green-flies) and the scale-insects. (b) ENDOPTERYGOTA, winged insects which have a complete metamorphosis (egg, larva, pupa, adult) with a resting pupa (or chrysalis). NEUROPTERA — lace-wings, alder-flies, scorpion-flies. TRiCHOPTERA — caddis-flies, with aquatic larvae and moth-like adults with hair-covered bodies and wings. LEPIDOPTERA — butterflies and moths. COLEOPTERA — beetles, including over 200,000 known species, both terrestrial and water-beetles. STREPSiPTERA — Stylops, miuvitc insects, parasitic on other insects, particularly wasps and bees. HYMENOPTERA — gall-flies, saw-flies, ichneumon-flies, bees, wasps, ants. DIPTERA — two-winged flies, midges, gnats, mosquitoes and frviit-flies. APHANiPTERA — the secondarily wingless fleas (jiggers, etc.), blood- sucking in habit and parasitic on birds and mammals. Ill the larval form all insects possess simple lateral eyes (stemmata; ardixixy., a garland). The adult also frequently possesses simple eyes (DOES.\f. ocelli), although they are absent or vestigial in many species, as in rt.ost beetles and mosquitoes, some families of flies, and noctuid moths nt in addition it is provided with multifaceted compound EYES. his generalization there are some exceptions in degenerative ARTHROPODA 221 forms which are unprovided with compound eyes — the primitive wingless Collembola (Fig. 223), hce and parasitic fleas which possess only ocelli (Fig. 224), while species which live in darkness may be iniprovided with eyes, such as the Protura, the driver ant of Africa, Dorylus (with the exception of the winged male), or most termites. The winged male Stylops has aggregate eyes composed of a multitude of ocelli so closely packed together as to resemble a compound eye, but the parasitic female Mhich passes its whole life within its host, is unprovided with eyes.^ jVIale driver ant Figs. 22.3 and 224. — Insects with Ocelli and Xo Compound Eyes (Xatural History Museum, London). Fig. 2l':;. Tlic springtail, Arrhi.stoiuti brs-selsi (Collem- bola). There are 8 ocelli on each side and no compound eyes. Fig. 224. — The bird-louse, Trinoton acidenlioii (Anoplura). There are 2 simple eyes (S) on each side and no compoimd eyes. We shall see ^ that the compound eyes are the dominant organs in the adult insect, the simple eyes essentially accessory ; this is .seen in the occasional disappearance of the latter as the former develop. Thus the larva of the water-beetle, Dytiscus, has 6 ocelli on each side of the head, but in the later stages of larval development the compound eye appears in front of them, first as a crescentic area on each side. At the stage of moulting the cornea^ of the ocelli are shed with the cuticle and as the compound eye rapidly develojDs the bodies of the ocelli recede, remaining, however, permanently attached in vestigial form to the optic nerves, 1 For the descriptive anatomy of the compound eyes of Insects, see p. 166 ; for that of the ocelli, see Hesse (1901), Merton (1905), Link (1908-9), Strohm (1910), Demoll and Scheurins (1912). Bugnion and Poiwff ( 1914), Melin (1923). Homann (1924), Hamihon (1925), Zikan (1929), Wolsky (1930-31), Friederichs (1931). Verrier (1940), Lhoste (1941). ^ p. 224. Female driver ant Stylops 222 THE EYE IN EVOLUTION Figs. 225 to 227. — The Compound Eyes of Insects. Fig. 225. — The head of the dragon-fly, jEschna californica (Odonata) capped by two enormovis crescent-like comiDound eyes (James Needham). Fig. l&.- -The male gadfly, Ancnia fasciata nilotica (Diptera). The immense compound eyes occupy the whole of the surface of the head (Natural History Museum, London). Fig. 227. — The cave-bug, Leotichius glaucopis (Hemiptera). From Malaya. Dorsal surface. The 2 prominent compound eyes (C) are largely spread over the ventral surface. There are 2 median ocelli (S) (Natural History Museum, London). THE STEMMATA (OR LATERAL OCELLi) OF LARVAL OR PUPAL FORMS can in general be classified into two main types. The most elaborate organs are seen in the larvae of Lepidoptera and Trichoptera ; these are arranged in a group of variable size ^ on either side of the Jjcnd, each separate individual of which takes the form of the single itnatidium of a compound eye with a cuticular corneal lens, g., 6 on either side of the head in the caterpillars of butterflies. ARTHROPODA 223 Figs. 228 and 229. — Stalked Compound Eyes. Fig. 228. — A grouse locust, Ophiotettix limosina (Orthoptera). ' The compound eyes (C) are placed on either side at the end of the stalk- like head. (One antenna is missing.) (Natural History Museum, London.) Fig. 229. — The stalk-eyed fly, Achias rothschildi (Diptera). The lai'ge compound eyes (C) are at the end of unusually long stalks (Natural History Museum, London). a crystalline cone and a retinule of 7 sensory cells grouped around a rhabdome (Fig. 138) (Dethier, 1942-43). A more simple variety is seen in the larvae of Tenthredinidffi (saw-flies) and Coleoptera. These usually have two lateral eyes of cupulate shape with a retma formed as a palisade of sensory cells under a lens -like thickening of the cuticle. The retinular cells are arranged in groups of two or three, each group around an elementary rhabdome which is not constructed for the reception of images. More rudimentary forms occur such as the Sawfly 224 THE EYE IN EVOLUTION simple pair of visual cells with two overlying pigment cells which form the eye of the larva of the midge, Ceratojjogon, or the few light-sensitive cells lying in a shaded pocket in the pharyngeal skeleton of the larva of the house-fly, Musca (Fig. 99) (Welsh, 1937 ; Debaisieux, 1939). THE DORSAL OCELLI OF ADULTS were described and figured as early as 1678 by the French scientist, de la Hire (Figs. 149, 227, 230). They are usually three in number arranged in triangular form, one median and anterior and two lateral and posterior on the dorsal aspect of the Figs. 230 and 23 L — Unusual Compound Eyes in Insects (Natural History Museum, London). Fig. 230. — The aphid, Dnctynotus obscuras (Homoptera). There are 2 compound eyes (C) one on each side of the head, and, in winged forms, 3 ocelh on tlie vertex of the head, the median one of which is marked S. In the family Aphididae there is in addition a prominence, the triommatidion (T), of unknown func- tion, bearing 3 facets at the base of each compound eye. This organ is always present, even in those forms in which a comjjound eye is lacking. Fig. 231.— The Whirligig beetle, Dineutus grossus (Coleoptera). There are 2 compound eyes on each side of the head, one dorsal (D) for aerial vision, and one ventral (V) for vision under water. head between the compound eyes ; but they are small and incon- spicuous, being often hidden by scales as in moths or hairs as in bees. In some species of ants belonging to the sub-family Myrmicinae, the anterior ocelli are double or binary in type (Weber, 1947). In others, such as Orthoptera, the ocelli are vestigial ; in general, their degree of development shows some correlation with that of the wings (Kalmus, 1945). As a rule they resemble in structure the more simple type of stemmata, being comjirised merely of a group of visual cells associated with rb-'bdomes lying beneath a common cuticular lens (Fig. 108). T OMPOUND EYES OF ADULTS are laterally situated on the head and foi be essential visual organ (Fig. 149). They are large and ARTHROPODA 225 prominent and vary in complexity from the small organ of the worker of the ant, Solenopsis. which lives underground and is provided with 6 or 8 facets, to the elaborate organ of dragon-flies (Odonata) with up to 28,000 1 ommatidia (Imms, 1935) (Figs 225 to 227). Occasionally the compound eyes are enormous, literally occupying the whole surface of the head, as is seen in the gad-flies (Tabanida?) (Fig. 226) ; usually they are situated on the surface of the head, sometimes they stand out prominently as in the praying mantis (Fig. 734), but occasion- ally they are perched on long stalks (Figs. 228 and 229). Exceptionally two compound eyes are differentiated in function, such as in the whirligig beetle, Dineutus, which has a dorsal compound eye for aerial vision and a ventral for vision under water (Fig. 231).- A unique organ is seen in the Aphid family (" green-fly ") in which an additional tri- faceted organ, the triommatidion, is found at the base of each compound eye (Fig. 230) ; the function of this organ is imknown but it is present even in those forms of aphids which have no compound eyes. von Buddenbrock, Moller-Racke and Schaller. Experientia, 10, 333 (1954). Biitschli. Vorlesungen ii. vergl. Anrit., Berlin, 872 (192'l). Bugnion and Popoff. Arch. Anat. inter., 16, 261 (1914). Caesar. Zool. Jb., Abt. Anat., 35, 161 (1913). Constantineanu. Zool. Jb., Abt. Annt., 52, 253 (1930). Dakin. Quart.J.»ilcr.Sci..6b, 163(1921). Debaisieux. Ann. Soc. Sci., Bruxelles, 59, 9 (1939). DenioU. Die Sinnesorgane der A rthropoden, Braunschweig (1917). Demoll and Scheuring. Zool. Jb., Abt. Zool. Physiol., 31, 519 (1912). Dethier. J. cell. camp. Pltysiol., 19, 301 (1942) ; 22, 115 (1943).' Dijkgraaf. Z. vergl. Phi/siol., 38, 491 (1956). Exner. Die Physiologic d. Jacetlicrten Augen von Krebsen u. Insekten, Leipzig (1891). Fales. Biol. Bull., 54, 534 (1928). Friederichs. Z. Murphol. Oekol. Tiere, 21, 1 (1931). Graber. Arch. mikr. Anat., 17, 58 (1880). Grenacher. .-^rch. mikr. Anat., 18, 415 (1880). Zool. An: Hamilton. (1925). Hanstrom. (1926). Harris and Mason 280 (1956). , 18, 280 (1895). Publ. U.S. nat. Mus., 65, 1 Lunds I Aarssr, 22 Proc. toy. Soc. B., 145, 1 p. 172. Hentsfhel. Zool. Jb., Abt. Anat., 12, 509 (1899). von Hess. Vergl. Physiol, d. Gesichtssinnes, Jena, 79 (1912). Hesse, R. Zool. Anz., 24, 30 (1901). Das Sehen der niederen Tiere, Jena (1908). de la Hire. Mem. Acad. roy. Sci. Paris (1666-1699), 10, 609 (1730). Homann. Z. vergl. Physiol., 1, 541 (1924) ; 7, 201 (1928) ; 14, 40 (1931). Zool. Jb.. Abt. Anat., 71, 56 (1950) ; 72, 345 (1952). Biol. Zbl., 72, 373 (1953). Imms. Textbook of Entomology , London (1935). Kalmus. Proc. roy. entom. Soc. Lond., A, 20,84(1945). Kor.schelt and Heider. Vergl. Entwicklung. d. Wirbellosen Tiere, Jena, 664 (1893). Lang. Zool. Jb., Abt. Anat., 21, 453 (1905). Lankester and Bourne. Quart. J. micr. Sci., 23, 177 (1883). Lhoste. Bull. Soc. zool. Fr., 66, 62 (1941). Link. Zool. Anz., 33, 445 (1908). Zool. Jb., Abt. Anat. ,2,1, -m, 281 (1909). Melin. Zool. Bidrag Uppsala, 8, 1 (1923). Merton. Z. iviss. Zool., 79, 325 (1905). Millot. Grasse's Traite de Zool., Paris, 6, 295, 533, 589, 698 (1949). Morgan. Biol. Stud. Johns Hopk. Univ., 5, 49 (1891). Muller, J. Zur vergl. Pliysiol. des Gesichts- sinnes des Mensclien it. d. Thiere, Leipzig (1826). Dragon-fly Whirligig beetle Aphid - Compare the eye of Anableps, p. 324. S.O. — VOL. I. 15 226 THE EYE IN EVOLUTION Parker. Bull. Mus. Comp. Zool., 13, 173 (1887). Patten. Quart. J. micr. Set., 35, 1 (1893). Petrunkevitch. J. exp. Zool., 5, 275 (1907). Zool. Jb.,Abt.Syst. Biol., Zl, 355 {Idll). Police. Zool. Jb., Abt. Anat., 25, 1 (1908). Purcell. Z. wiss. Zool., 58, 1 (1894). Radl. Pflugers Arch. ges. Physiol., 87, 418 (1901). Savory. The Biology of Spiders, London (1928). Scheuring. Zool. Jb., Abt. Anat., 33, 553 (1913) ; 37, 369 (1914). Schlottke. Z. mikr. Anat. Forsch., 32, 633 (1933). Sehulz. Z. vergl. Physiol. ,1, 488 (1928). Sokolow. Z. wiss. Zool., 98, 339 (1911). Strohrn. Zool. Anz., 36, 156 (1910). Tompsett. Liverpool marine biol. Comm. Mem., 32, 1 (1939). Vaissiere. C. R. Acad. Sci. (Paris), 238, 942 (1954) ; 240, 345 (1955). Verrier. Bull. Biol. France Belg., 74, 309 (1940). Versluys and Demoll. Ergebn. Fortsch. Zool. Jena, 5, 67 (1923). Weber. Biol. Bull., 93, 112 (1947). Welsh. .Sczence, 85, 430 (1937). Widmann. Z. wiss. Zool., 90, 258 (1908). Wolsky. Z. vergl. Physiol., 12, 783 (1930) ; 14, 385 (1931). Biol. Bev., 8, 370 (1933). Zikan. Zoo/, ylnz., 82, 269 (1929). CHAPTER VIII THE EYES OF PROTO-CHORDATES The Chordates constitute a phylum characterized by a dorsal tubular nerve-cord, a dorsal supporting axis (a notochord) and pharjTi- geal gill-slits ; the last two, however, may be temporary in duration. The Vertebrates constitute a sub-phylum within the Chordates which possesses as distinctive characters a head and skull, a brain with eyes, a vertebral column, and (generally) paired limbs. Stumbling on the FiG. 232. — B.iLAyoGLOssvr. The long tongue-like proboscis (Pr) resembles an acorn (/3aAo(i'Of, an acorn ; yXioaax, a tongue). border-line between Invertebrates and Vertebrates are three classes of animals (Proto-chordates) possessed of a rudimentary nerve-cord, a notochord and gill-clefts — the Hemichordates, the Tunicates, and the Lancelets. Apart from the pelagic Tunicates, these lowly creatures are either sessile or burro\\ing in habit. The HEMiCHOEDATA are typified in Balanoglossus, a worm-like marine creature burrowing in the sand and mud of most seas (Fig. 232). Fig. 233. — The Eyes in the Tornaria Larva of Bala.\oolossvs. Antero-posterior section through the apical plate showing the anterior, EA, and posterior, EP, eyes (after Morgan). The nervous system arises as a longitudinal groove of ectoderm which becomes tubular but gives no evidence of visual out-pouchings. In the larv£e (tornaria) of some species situated on the apical plate there are two eye-spots consisting of cup-shaped depressions of clear cells surrounded by pigment (Fig. 233), but in the adult there are no special sense organs (Spengel, 1893 ; Stiasny, 1914). 227 228 THE EYE IN EVOLUTION Fig. 234.— The Sea- squirt, ascidia. The adult covered by its tunic (test), the lower end attached to a rock, the upper end ending in an inhalant siphon (mouth), and on the mor- phological dorsal surface an exhalant sijshon (atrial opening). Around both apertures thei-e are sometimes jDigment spots of unknown character. During life, the animal draws water in through the first and expels it from the second ; if irritated, water is forci- bly expelled from both, hence the name " sea- squirt." The TUNiCATA (urochordata) are typified in the Ascidians or sea-squirts (Fig. 234). Ascidia in its free-swimming larval stage is a tadpole-like creature, about 1"0 mm. in length, possessing the chordate characteristics of a brain and a dorsal tubular nervous system, a notochord and gill-slits. At this stage it is provided with a single cerebral eye associated with a statocyst, but as the hermaphroditic adult settles to its sedentary plant-like life within its thick tunic of cellulose and attaches itself to rocks or weeds, the nervous system is reduced to a single ganglion above the pharynx and the eye disappears. In some of these forms the siphons respond to light by retraction. It is true that pigmented spots are found around the siphonal openings, which used to be con- sidered " ocelli", but in Ciona, at any rate, they are in fact not light-sensitive (Millott, 1957). The transient eye of the larval Ascidian is of un- usvialmterest (Kowalevsky, 1871 ; vonKvipffer, 1872 ; Froriep, 1906). It arises as an out-pouching of the cerebral vesicle which forms a single sensory organ consisting of a sac containing a statocyst and an extremely elementary eye on its dorso -posterior wall (Fig. 235). The retina is composed of a few sensory cells derived from the inner wall of the neural tube ; it is capped with pigment and above it lies a rudi- mentary cellular lens. It is interesting that the visual cells are morphologically inverted inasmuch as they face towards the cavity of the sensory vesicle while the intrinsic lens faces towards the brain as if it would be effective only for light traversing the transparent body of the animal. In free -swimming Tunicates visual organs may persist ; thvis in the asexual form of Salpa there is a single median horse-shoe-shaped ocellus and some- times smaller accessory ocelli on the dorsal aspect of the animal closely associated with the single nerve ganglion. The LANCELETS (ACRANIA ; CEPHALO- chordata) are variously regarded as a pioneer off-shoot from the chordate stock or as a degenerate member of the phylum. They possess a dorsal tubular nerve-cord, a notochord and giU slits but lack a differentiated brain or eyes. T" - are typified in the common lancelet. Fig. 235. — The Eye of THE ASCIDIAN TaDPOLE Diagram of the sensory vesicle with a unicellular otolith and an ocellus (above right) with retinal cells, pigment and 3 lens cells situated towards the cavity of the vesicle (Ber- rill, The Origin of Verte- brates, Oxon., 1955). PROTO-CHORDATES 229 Branchiostoma (Amphioxus) lanceolatum, a small translucent fish-like marine creature about 2 in. in length the body of which is divided into 62 myotomes (Fig. 236). Although possessing no definitive eyes, the animal is strongly photo -negative and sensory organs occur, some possibly in the surface ectoderm and others deeply placed in relation to the neural tube which tend to enforce upon the animal its burrowing habit. Fig. 236. — The Lancelet, Amphioxus. The head end is towards the right, the tail end to the left (after Haeckel). The superficial sensory organs are the large isolated cells of Joseph (1904-28), associated with the surface eiaitheliuni on the dorsal aspect, which were claimed by this investigator to be light-sensitive (Fig. 237) ; this view, however, is by no means substantiated. The neural photosensitive organs are of two types (Fig. 237). Towards the cephalic end of the animal a small median area of ependymal cells lining the central canal of the nerve-cord is specially differentiated to form an infundi- bular ORGAN which appears to be light-sensitive and is functionally allied to a Fig. 237. — Sagittal Section of the Anterior Portion of Amphioxus. CJ, cells of Joseph ; Inf, infundibulum ; NC, neural oanal ; PS, anterior pigment spot (after Boeke). dark pigment -spot situated at the head end of the animal. The pigment-spot was originally described as an " eye-spot " by Johannes Miiller in 1842, and used to be credited with light-sensitive properties and specific connections with the central nervous system ^; it was indeed held to be the phylogenetic precursor of the vertebrate eye. Its specific innervation, however, was contested initially by Kohl (1890) and conclusively by Fi-anz (1923), and a visual function excluded 1 See the writings of W. Miiller (1874), Langerhans (1876), Ayers (1890), Joseph (1904-28), Edinger (1906), Boeke (1908), Pietschmann (1929). 230 THE EYE IN EVOLUTION by the experiments of Nagel (1896) and Hesse (1898) and more particularly by those of Parker (1908) and Crozier (1917). There would seem little doubt that it is not a vestigial eye but that its function is to endow the infundibular organ with directional ability by casting a shadow upon it when the animal or the light source moves, a primitive role we have already seen in the eye -spot of the Protozoon, Euglena ^ (Franz, 1912-34 ; WoUenhaupt, 1934). A second jDhotosensitive mechanism is seen in the ORGANS OF HESSE (1898), individual cells scattered on the ventral and lateral aspects of the nerve-cord to- wards its posterior end (Figs. 238 and 239). These are single large ganglion cells variously orientated, each provided with a brush-like ciliated margin and an issuing nerve-fibre, each capped by a crescent-shaped pigment cell to give it directional a.bility. The distribution and structure of these unique cells have been fully studied by a number of observers (Franz, 1923 ; Joseph, 1928 ; Kolmer, 1928 ; WoUenhaupt, 1934) and their photosensory function established by Parker (1908) and Crozier (1917). Fig. 238. — Visual Cell of auphioxvs. n, nucleus ; c, striated margin ; p, jjigment mantle. Fig. 239. — The Neural Visual Cells of Amphioxus. Section through the sj^inal cord in the region of the 5th segment, showing the central canal, C, and the large visual cells of Hesse, H, with their associated pigment cells (after Hesse). Ayers. ZooZ. ^Inz., 13, 504 (1890). Boeke. Anat. Anz., 32, 473 (1908). Crozier. Anat. Rec, 11, 520 (1917). Edingef. Anat. Anz., 28, 417 (1906). Franz. /?-o/. Zbl., 32, 375 (1912). Jena. Z. Natzirw., 59, 401 (1923). Bolks . Berl,. vergl. Anat. d. Wirb'lliere, (ii), 989 (1934). Froriep. Handbuch d. vergl. und exper. Entwicklungslehre d. WirbeUiere, Jena, 2 (1906). Anat. Anz. (suppl.), 29, 145 (1906). Hesse. R. Z. wiss. ZooL, 63, 456 (1898). Joseph. Anat. Anz. (suppl.), 25, 16 (1904). Biol, generalis, 4, 237 (1928). Kohl. Zool. Anz., 13, 182 (1890). 126. PROTO-CHORDATES 231 Kolmer. Biol. generaUs, 4, 256 (1928). Kowalevsky. Arch. wikr. Anat., 7 101 (1871). von Kupffer. Arch, tnikr. Anat., 8 358 (1872). Langerhans. Arch. mikr. Anal., 12. 290 (1876). Millott. Endeavour, 16, 19 (1957). Miiller, J. Abh. Kgl. Akad. Wiss., Perlin (1842). Muller, W. V. d. Stamme.sentivicklunq d. Sehorgans d. Wirbelthiere, Leipzig (1874). ^ ^ Nagel. Der Lichtsinn uugenloser Tiere : eine biologi.<Dipnoi Coelacanths {Latimeria) f;"":;^ lExtant Urodela > . , ., . Apoda J Amphib.a -Chelonia\ Therapsida | Sauropsida->Sp/ienodon Lizards and snakes Extant Reptiles 4 MAMMALS Archosauria -> Croco- (Dinosaurs) diles I BIRDS EXTINCT VERTEBRATES (Drawn not to scale but to standard size) Agnathous Fishes Pteraspis Cephnlaspis Placoderm Rhipidistian Prinutive Ampb ■ '-n Primitive Reptile Dinosaur, Diplodocus THE VERTEBRATE EYE 235 Cyclostomes, the lamprey and the hag. From these there evolved somewhere in the Upper Silurian period, 350 million years ago,^ the true (gnathous) fishes, possessed of jaws and paired fins. From these primitive fishes three classes radiated : (1) the Placoderms, a motley class mostly with bony armour, which flourished in Devonian times but none of which survived the Palaeozoic era ; (2) the Chondrichthyes, a class of cartilaginous fishes of great age which are now represented only by the Selachians (sharks and rays) and Holocephalians (deep- sea chimtpras) ; and (3) the Osteichthyes, the much larger class of bony fishes. While the Placoderms have disappeared, and the cartilaginous fishes, prolific in the older geological periods, have steadily decreased in importance in more recent times, the bony fishes have shown themselves remarkably adaptive. By the end of the Palceozoic era they had attained almost sole possession of fresh-water streams and lakes ; at that time they had invaded the sc^^s also and rapidly constituted the vast majority of marine forms. These bony fishes may be divided into two main sub-groups, each of which has numerous survivors : the Actinopterygii and the Crossopterygii. From the former a series of forms arose in linear progression — the Chondrostei, still with a largely cartilaginous internal skeleton, degenerative representatives of which still survive as the Polypterini (two species of which are extant) and the sturgeons ; the Holostei, provided with bony skeletons, represented today only by two American fresh-water fishes, the bow-fin and the gar-pike ; and eventually the Teleostei, the most specialized of all fishes which include practically all modern species. From the early Crossopterygii the Dipnoi (lung-fishes) appeared as an aberrant off-shoot in the lower Devonian period ; of these, three species survive today, swamp -dwelling, mud-loving and eventually air-breathing fishes in which the swim-bladder has been retained as a functioning lung. From the main group, however, a direct line of vertebrate descent continued through the Rhipidistia (a derivative of which exists today as the Coelacanth, Latimeria) ; these fish could already breathe air so that they only had to turn their fins into legs and modify the ear to become Amphibia and survive on land. Develop- ing as tadpole-like aquatic creatures, they underwent this remarkable meta- morphosis as they matured into their adult forms. Initially they lived side-by- side with their cousins, the lung-fishes, in the swamps ; but when the great droughts appeared and the fresh-water pools dried up towards the end of the Devonian period some 300 million years ago, the lung-fishes largely perished, but the Amphibians, capable of creeping and feeding on land, survived. Their first representatives have long become extinct and the class survives today only in three relatively unimportant and highly specialized groups — the frogs and toads (Anura), the salamanders and newts (Urodela) and the worm-like Cfecilians (Apoda). From the highly adaptable primitive types, however, there evolved in the Upper Carboniferous period the first fully terrestrial verte- brates, the most primitive Reptiles, born on land and capable of existing away from water altogether. This spectacular step in evolution was made possible by the development of a large and highly nutrient egg protected by a porous shell so that the young reptile could emerge fully equipped for terrestiial life. For many millions of years these primitive reptiles fiourished exceedingly ; emerging on to the hitherto unexploited land, rich in vegetation and food, they spread and gave rise to a multitude of new types, some of them of incredible form and giant size. They still retained, however, the cold-blooded characteristic of their fish and amphibian ancestors, and thus, presumably owing to the climatic changes at the end of the IMesozoic era, this group which had dominated the 1 See p. 754. 236 THE EYE IN EVOLUTION earth for more than 100 miUion years perished, apart from a few unimportant exceptions — the very primitive Chelonians (tortoises and turtles), the almost extinct Rhynchocephalian, Sphenodon, of lineage almost as remote ; and the more modern groups, lizards and snakes and crocodiles. The handicap of cold-bloodedness limited these surviving Reptiles to the warmer parts of the earth. In the even temperature of the sea the Teleosteans could flourish without hindrance ; to populate the cooling earth homeostasis had to be achieved ; this was eventually acquired by Birds and Mammals, the former assuming an insulating coat of feathers, the latter usually of hair in place of the scales characteristic of Reptiles. Of the two the Mammals claim the more primitive descent, stemming from the Therapsidans, mammalian- like Reptiles which flourished in Permian and early Triassic times. During the latter period it would seem that Mammals made their appearance as small mouse-sized creatures, but throughovit the entire Mesozoic era they appear to have been sparse, leaving few fossil remains ; it was not until the end of the Cretaceous period, 75 million years ago, when the great carnivorous Reptiles finally died off that these retiring, inconspicuous creatures, probably nocturnal or arboreal in habit, were able to take the leading place in evolvitionary progress. This they have done to such good purpose that they have adapted themselves to and become completely predominant in almost every environment on land, some of them even returning to the water wherein their lately acquired superiority afforded them a relatively easy existence (whales, seals, Sirenians) while others (bats) have invaded the air. Parallel with the Therapsida stands the other reptilian group of Sauropsida, of which lizards and snakes are a direct off-shoot ; from it was derived the Archosauria, a group characterized by a limb-and-girdle structure enabling them to run semi-erect upon their hind legs with a bipedal gait. The only members of this stock which have survived are the crocodiles and their relatives the alligators ; but, particularly in their most spectacular forms, the Dinosaurs, some of them as heavy as 40 or 50 tons, they constituted the dominant terrestrial type during the latter half of the Mesozoic era. From these are descended modern Birds which show innumerable reptilian features. Curiously it was from the most primitive type of placental Mammal, the Insectivores, that the Primates and Man evolved, and in the evolution of these the great advance has been associated with the brain. This was achieved in a peculiar way. A small and unimportant group became adapted to arboreal life, thus developing their cortical capacity by the coordination of the eye and hand ; thereafter, descending from the trees and freeing their hands by becoming bipedal, they passed the critical point at which physical dexterity could combine with conceptual thought and the faculty of speech, and thus a new method of evolution became possible based on the transmission of cultural experience. At this stage the potentialities of vision are measured not by the optical and structural excellence of the receptive end-organ, but by the apperceptive capacity of the mind. In this way, just as the Mammals defeated the lower Vertebrates on land, leaving the water to the Teleosts and the air to the Birds, so the Placentals eliminated the Monotremes and Marsupials wherever they came in contact with them, the Carnivora dominated the lower Placentals, the monkeys the Prosimians, and finally Man triumjihed over all the others. From the anatomical point of view — and certainly from the aspect of the structure of the eye — these six classes of the Vertebrates, neglecting the Cyclo- stomes, can conveniently be reduced to three great groups as suggested by Huxley : THE VERTEBRATE EYE 237 1. The ICHTHYOPSIDA — Fishes and Amphibians, the primary habitat of which is water — completely so in the case of the first and developmentally so in the second. Although the eyes of adult Amphibians show many terrestrial adaptations, the larval stage is spent in water and the adjustments for aerial vision are added to the general plan of the aquatic eye. 2. The SAUROPSIDA — Reptiles and Birds which, despite the difference in their external appearance, show many close structural affinities. In them the eyes have become completely adapted to aerial vision. 3. The MAMMALIA, in which the eye, starting from a primitive reptilian source, has developed along separate lines adapting itself to almost every environmental habitat — including a return to aquatic vision. THE PHYLOGENY OF THE VERTEBRATE EYE We have already seen that the eyes of Invertebrates are developed from the surface ectoderm and that the visual cells are connected to the nervous system secondarily ; the eyes of Vertebrates, on the other hand, arise from the neural ectoderm. It is true that the neural ectoderm itself is ultimately derived as an infolding from the surface layer, but the cerebral eye of Vertebrates indicates a major evolu- tionary step affording the sentient layer of cells all the opportunities for the pluripotential differentiation characteristic of the central nervous system of which in every sense it forms an integral part. An apparatus capable of subserving a highly developed sense of vision depends no less on the efficiency of its central nervous representation which interprets its images than on the peripheral sensory apparatus which receives and resolves them. Moreover, an endoneural receptor immune because of its position to other stimuli, mechanical or chemical, can evolve a delicacy of response without danger of false alarms that could not be attained by an organ exposed on the surface. The significance of the origin of the vertebrate eye is thus apparent ; the process is essentially the same as in Invertebrates, both the eye and the central nervous system being ectodermal, but in the latter the eye has evolved from the surface ectoderm primarily, in Vertebrates it is secondarily derived.^ The curious thing, however, about the evolution of the vertebrate eye is the apparent suddenness of its appearance and the elaboration of its structures in its earliest known stages. There is no long evolutionary story as we have seen among invertebrate eyes whereby an intracellular organelle passes into a unicellular and then a multicellular eye, attaining by trial and error along different routes an ever-increasing degree of complexity. Within the vertebrate phylum the eye shows no progress of increasing differentiation and perfection as is seen in the brain, the ^ It is to be noted that the sensory cells in the epidermis of the tail of the ammocoete larva of the lamprey are probably light-sensitive (Steven, 1950-51) ; they resemble the apolar light cells seen in some worms (Lumbricu.s) and molhiscs (Mya) (p. l.*^!). This is the only instance of the occurrence among Vertebrates of the primitive light cells characteristic of Invertebrates, and is analogous (perhaps) with the cells of Joseph seen in the integument of Amphioxus (p. 229). 238 THE EYE IN EVOLUTION ear, the heart and most other organs. In its essentials the eye of a fish is as complex and fully developed as that of a bird or man ; the differences between the members of the series are relatively minor in character, adaptations to the habits of the animals rather than expressions of phylogenetic evolution. All Vertebrates have a three- layered retina and a pigmentary epith&lium, all have the same dioptric apparatus of a cornea and an epithelial lens, all have the same nutrient mechanism. It is true that the essential visual components except the three-layered retina are found in many invertebrate eyes ; but at the same time it is to be remembered that the optic ganglion of the latter group corresponds essentially to the nervous layers of the retina of Verte- brates. Despite these similarities, however, a revolution has taken place. Throughout the whole phylum paired lateral eyes are present, although occasionally, as in specialized predators such as the hagfish, Myxine, or in cave-dwelling or abyssal fishes, subterranean amphibians and reptiles and the mole, they may degenerate.^ In the most primi- tive vertebrates known to man — the long extinct agnathous fishes {Pteraspis, Cephalaspis, etc.) the fossil remnants of which are found in the rocks of the Silurian era ^ — a median and two lateral eyes were present. In the extant representatives of this primitive stock, the lampreys (Petromyzon), the lateral eyes are rudimentary and hidden in the arnmocoete (larval) stage ; but in the adult they become well- developed and reach the surface (Figs. 276-7), while the animal is also provided with median pineal and parietal " eyes ".^ Although primitive, however, and lacking the diagnostic characteristics of true fishes, the lateral eyes of this most primitive type emerge as fully differentiated organs and shed little light on the origin of the eyes of the higher species. It would seem, therefore, that the vertebrate eye evolved not as a late off-shoot from the simple eye of Invertebrates after the latter had reached an advanced stage ; it probably emerged at a very early stage, further back than geological evidence can take us, and developed along parallel but diverging lines. The apposite remark of the great German anatomist, Froriep (1906), that the vertebrate eye sprang into existence fully-formed, like Athene from the forehead of Zeus, expressed the frustration of the scientists of half a century ago to account for its appearance ; today we are little wiser. The apparently revolutionary changes in morphology which characterize Vertebrates are not, of course, confined to the eyes. The abruptness of the separation between the backboned and backboneless animals -Aab evident to Aristotle and was firmly drawn by Lamarck in 1801), but the pedigree of the former — presumably from the latter — still ren! V '^s unknown and all the theories which have been advanced ^ p. 72i. 2 320 to 350 million years ago, p. 754. * p. 713. THE VERTEBRATE EYE 239 are suggestive rather than convincing. Moreover, in the case of a soft organ any help from fossil types is lacking. We are therefore driven to seek what evidence we can from ontogeny. Froriep. Hb. d. vergl. u. exper. Entwick- Romer. Vertebrate Paleontology, Chicago lungslehre d. Wirbeltiere, Jena, 2 (1947). (1906). Steven. J. exp. Biol., 27, 350 (1950). Quart. J. micr. Sci., 92, 233 (1951). Anat. Anz. (buppL), 29, 145 (1906). Trewavas, White, Marshall and Tucker. Lamarck. Zoological Philosophy (1809). Nature (Lond.), 176, 126 (1955). THE ONTOGENY OF THE VERTEBEATE EYE Ontogenetically, the central nervous system first appears as a superficial groove along the mid-dorsal line of the embryo which eventually invaginates,i the anterior part to form the anlage of the brain, the remaining and greater part to form the spinal cord. At an early stage before the closing-in process occurs, the anterior cephalic end grows more rapidly than the rest and forms three primary vesicles, ^ and at the cephalic end of the rudiment of the forebrain, tucked into a recess at each corner, a paired lateral depression appears, known as the optic pits {foveolce opticce). These paired pits, lying on the surface of the open cephalic plate, have been seen on the surface of many types of embryos in some of which they are pigmented (Froriep, 1906 ; Lange, 1908 ; Franz, 1934 ; and others) (Figs. 242 to 247). As the neural groove invaginates to become the neural tube, the optic pits become invaginated with it to form the primary optic vesicles, which, reaching the surface as lateral out-pouchings of the cerebral vesicles, again invaginate to form the secondary optic vesicles (or optic cups). In all Vertebrates the retina participates in the high degree of differentiation which characterizes the central nervous system. The proximal wall of the optic cup remains as a unicellular layer and acquires pigment to form the pigmentary epithelium, but its inherent plasticity is seen in the capacity of the amphibian epithelium to regener- ate an entirely new functional retina if the inner layer is removed (Stone, 1950). The neuro-epithelium which forms the distal layer of the cup, like that which determines the cerebral and cerebellar cortex, differentiates into three strata — a marginal zone of ganglion cells, an intermediate mantle zone (bipolar, amacrine, horizontal and ^ The fact that the nerve-cord in Amphioxus first appears as a solid rod which canalizes at a later stage has suggested to some authorities that this sequence represents a phylogenetic step in the evolution of the central nervous system of Verte- brates ; but it is to be remembered that the evidence indicates that the Lancelets are an off-shoot of the main vertebrate stock rather than a primitive type. It is also to be noted that Graham Kerr (1919) described the forebrain of Lepidosiren and other fishes as developing in the form of a solid rod from which the optic vesicles grew as solid buds to become canalized later. This, however, is probably merely a question of the timing of various stages of development ; and no dogmatic judgment on this question can vet be given. 2 p. 532.' 240 THE EYE IN EVOLUTION Figs. 242 to 247. — The Ontogenetic Development of the Lateral EYE of VeBTEBRATES. Fig. 242. Fig. 243. Fig. 244. Fig. 245. Fig. 246. Fig. 242. — The appearance of the foveolae opticse ( / ) on the dorsal ectoderm of the cephahc (medullary) plate {m.p.). Fig. 243. — Invagmation of the surface ectoderm with the optical area to form the primitive neural tube. Fig. 244. — Evagination of the primary optic vesicle. Fig. 245. — The commencement of secondary invagination of the neural epithelium with thickening of the surface epithelium. Fig. 246. — Invagination of the surface epithelium. Fig. 247. — Detachment of the lens from the surface epithelium. Miiller's cells) and an outer zone of sensory cells, perhaps the linear descendants of the ependymal cells (rods and cones). In this way the strati I-! cation of cells with their accompanying system of interconnecting neurones allows the appearance of a complex conducting and associating appara 's. With very few exceptions the retina of Invertebrates is THE VERTEBRATE EYE 241 formed by a single ectodermal layer ; but into the retina of Vertebrates is thus aggregated the analogue of the ojitic ganglion of Invertebrates ; it becomes an island of the central nervous system, and the optic nerve becomes a tract of this system connecting the outlying part with the main body. In the vast majority of cases we have seen that the receptor end of the sensory cell in the epithelial eye of the Invertebrate lay towards the surface of the body/ but when it was enfolded in the neural tube of the Vertebrate, this end now lay deeply and the pole from which the nerve fibre issues became superficial (Fig. 247). It follows that in the cerebral eye of the Vertebrate, light must traverse the whole thickness of the retina in order to reach the sentient layer ; such an arrangement we have already called an inverted retina in contradistinction to the more primitive verted retina wherein light first strikes the visual cells before reaching their nervous prolongations.^ The inverted retina may seem an anomalous arrangement from an optical point of view, but it carries the advantage that the visual receptors can be brought into contact with the pigment and that the part of the retina in which the greatest activity occurs lies nearest the caj)illaries of the choroid ; both of these — pigment and a dense layer of blood-vessels^ — for optical reasons could only be situated deeply to the visual elements. More- over, an inverted arrangement allows the evolution of intracellular colour filters within the visual cells (Walls and Judd, 1933) and permits an increase of the resolving power of the central region by the formation of a fovea (Walls, 1937). The remainder of the eye is derived from the surrounding ecto- dermal and mesodermal tissues. The surface ectoderm devotes itself entirely to the formation of the dioptric apjDaratus. an arrangement which allows greater efficiency than was the case in Invertebrates in which a refringent mechanism was developed from the same layer as the sentient cells themselves. Intercalary cells in the sentient layer, however, retain this function to some extent by secreting a transparent medium (the vitreous). Organs of protection are provided from the surrounding mesodermal tissues — a fibrous sclerotic coat, lids, a lacrimal apparatus, and a bony orbit ; and from the same source a motor apparatus is added, and a vascular system provided. Franz. Bolk's Hb. d. vergl. Anat. d. Lange. Zbl. prnkf. Angeuheilk., 32, 131 Wirbeltiere, Berlin, 2 (ii), 989 (1934). (1908). Froriep. Hb. d. vergl. u. e.rper. Entwick- Stone. Anat. Fee, 106, 89 (1950). lungslehre d. Wirbeltiere, Jena, 2 Walls. Arch. Ophthal. (Chicago), 18, 912 (1906). (1937). .4no?. ^nz. (Snppl.), 29, 145 (1906). Walls and Judd. Brit. J. Ophthal., 17, Kerr, Graham. Te.rtbook of Embryology. 641, 705 (1933). London (1919). 1 p. 146, 2 p. 146. S.O.— VOL. I. IG 242 THE EYE IN EVOLUTION THE EMERGENCE OF THE VERTEBRATE EYE Since Wilhelm Miiller (1875) first put forward his view that the pigment-spot in Amphioxus represented the forerunner of the vertebrate eye, many hypotheses have been advanced to explain its sudden and pecuhar appearance, but even today no theory can be said to be completely convincing and each raises difficulties in interpretation. These theories we shall now briefly discuss. Ray Lankester (1880-90) was among the first to appreciate the importance of the cerebral origin of the vertebrate eye and reasoned that, with the visual cells buried in the central nervous system, the original pelagic pre -vertebrate must have been transparent, as indeed are Ascidians and Lancelets, so that the light could traverse their bodies. As the body became opaque the eye was then forced to travel nearer and nearer to the surface until eventually it became separated from it only by a layer of ectoderm which retained its primitive transparency. In this view the light-sensitive cells originally associated with the medullary tube migrated to the surface bringing with them their associated pigment cells, and were multiplied and differentiated to form the retina ; meantime, the surface epithelium in the correspond- ing area remained transparent and ultimately became differentiated to form the dioptric apparatus (cornea and lens). This view seemed a reasonable explanation of the phenomenon and was crystallized by Balfour (1881) who pointed out that although the retina appeared to derive from the brain it did not originate there but, like the photoreceptors of Invertebrates, was really of integumentary origin, appearing initially as patches of photosensory epithelium on the area of the dorsal ectoderm which happened to become involuted with the neural tube (Figs. 248 to 254). Such a theory accounted for the inversion of the retina as well as its cerebral origin — a characteristic unique among vertebrate sense organs. The concept that the vertebrate eye ultimately derives from the skin was supported by a number of in- vestigators,^ while Schimkewitsch (1921) carried the theory further by suggesting that the lateral eyes were merely a pair of a series of homo- logous pit-like sense organs, the more anterior of which Were photo- sensory, a series in which were included other evaginations of the roof of the diencephalon such as the pineal and parietal eyes. In these latter eyes there is no secondary invagination so that a verted retina is formed ; and Sleggs (1926) and Estable (1927) explained the secondary invagination of the optic vesicles as a positive evolutionary step taken in order that abundant nourishment might be available from the choroid to allow a high degree of differentiation and activity in the sensory mechanism. ^ 1 von Kennel (1881), Dohrn (1885), Keibel (1906), Froriep (1906), Lange (1908), Franz (! '] •-), and others. THE VERTEBRATE EYE The origin of the essential sensory cells, the rods and cones, has long remained a matter of dispute. Ever since the time of Scliwalbe (1874) they had been generally considered as neuro-epithelium. Kraiise (1875), however, originally put forward the suggestion that they Figs. 248 to 254. — Hypothetical Scheme fob the Phylogenetic Development of Vertebrate Eyes. 243 Fig. 248. Fig. 252 Fig. 249. Fig. 253. Fig. 250. Fig. 251. Fig. 254. Fig. 248. — Photosensitive ciliated ectoderm on the dorsal aspect. Figs. 249 and 250. — Invagination of the surface ectoderm to form the neural tube, carrying with it the photosensitive ectoderm. Fig. 251. — The formation of the neural tube enclosing the photosensitive epithelium as ependyma. Fig. 252. — Commencing evagination of the neural tube. Fig. 253. — The formation of one median and two lateral optic vesicles. Fig. 254. — Invagination of the surface ectoderm with secondary in- vagination of the lateral optic vesicles to form two lateral eyes with inverted retinse. The surface epithelium takes no part in the development of the median eye which forms its own dioptric apparatus (lens) in the distal part of the vesicle which itself does not undergo secondary invagination and thus forms a verted retina. were derived from the ciliated ependymal cells lining the neural tube, the cilia eventually forming the outer segments of the visual cells — a view, however, which he quickly withdrew (1876). The vast authority of these two pioneers in the histology of the visual organs long remained unchallenged, but t he view that this layer of cells might 244 THE EYE IN EVOLUTION be ependymal in origin, the receptor end being phylogenetically homologous with the single cilium of an ependymal cell, was revived by Leboucq (1909), a theory which was elaborated with great persuasive- ness by Studnicka (1912-18), and subsequently supported by Walls (1939) and Willmer (1953). In this view the phylogenetic homologue of the vertebrate retina may be assumed to be the infundibular organ of Amphioxus ^ ; but it must be remembered that any convincing phylogenetic sequence connecting the two is lacking. Figs. 25.5 to 258. — Boveri's Conception of the Development of the Vertebrate Eye from the Organs of Hesse of an Amphioxus- LiKE Ancestor. Fig. 255. — Symmetrical arrangement of the organs of Hesse with pigment cells facing the central canal. Fig. 256. — Evagination of the canal carrying with it the organs of Hesse. Fig. 257. — Invagination to form a sensory and pigmented layer. Fig. 258. — Secondary invagination of the lens vesicle (from Walls, after Boveri). Such a development would not be unique since modified flagellated cells of this type are also seen in other sensory organs such as the olfactory cells, the hair cells of the labyrinth, the cells of the taste-buds and lateral line organs ; and it is to be remembered that there is a considerable amount of evidence that the ependymal cells in the diencephalic region retain some photosensory properties in several species of Vertebrates - (von Frisch, 1911 ; Scharrer, 1928 ; Nowikoff, 1934 ; Young, 1935 ; Benoit, 1937 ; and others). Agreement on the ependymal origin of the visual receptors is, however, by no means universal and many investigators, following Schwalbe, believe that they are endoneural. Thus Boveri (1904) traced their origin from the ganglion-like cells of Hesse in an Amphioxus-hke ancestors In this view he was supported by Parker (1908-9), 1 p. 229. 2 p. 537. 3 p^ 230. THE VERTEBRATE EYE 245 Tretjakoff (1913), Hescheler and Boveri (1923) and Nowikoff (1932). It was assumed that these cells became orientated in a regular manner with their associated pigment cells towards the central canal, and then were carried towards the skin in company with paired lateral diverticuli of the neural tube (Figs. 255 to 258). It is to be noted that by this hypothesis the inversion of the retina and the position of the pigmentary epithelium are also well explained. Although objections have been raised to this conception, such as the lack of ontogenetic and phylo- gent^l- confirmation of any intermediate stages of the migration, the Figs. 259 to 262. -Froriep's Derivation of the Ascidian (and Verte- brate) Eye. Fig. 259. Fig. 260. Fig. 261. Fig. 259. — The hypothetical original exi.stence of two sensory vesicles with an external lens and verted retina. Fig. 260. — Involution of the neural tube showing a lens facing the neural canal and a verted retina. Figs. 261 and 262. — Degeneration of one eye of the original pair and migration of the lens to an external position. For siinijlicitj- the statocyst portion of the sensory vesicle is omitted. absence of Hesse's cells in the head-end of Amphioxus and the danger of phylogenetic deduction from a species which appears to be an off- shoot rather than a primitive t\^e, the theory is undoubtedly ingenious. On the other hand, a phylogenetic analogy with the vesicular eye of the ascidian tadpole ^ was suggested by Lankester (1880) and strongly advocated by Jelgersma (1906). Such an ascidian hypo- thesis had to meet the criticism that this eye is unpaired while the presence of a lens situated on the cerebral aspect of the retina is obviously an anomaly (Fig. 235). Froriep (1906), however, suggested that the first difficulty could be overcome if the apparently unpaired eye in reality represented one of a pair ; in support of his hy|3othesis he showed that it was situated asymmetrically towards the right and was balanced by a degenerate mass on the left which he interpreted as a 1 p. 228. 246 THE EYE IN EVOLUTION vestigial eye. He attempted to overcome the second difficulty by postulating a migration of the lens from the cerebral to the superficial aspect of the vesicle ; his conception of the evolution of the organ is seen in Figs. 259 to 262. If the vertebrate eye stems from an ascidian- like ancestor in this way, the formation of the tubular neural structure precedes sensory differentiation, and any superficial sensory organ asso- ciated with the surface ectoderm must be assumed to disappear and be re- placed by the establishment of a neural photosensory organ. Why the dor- sal and lateral areas of the neural tube should show this photosensitive differentiation raises a difficult problem ; as occurs in many Inverte- brates, the tendency may be associated with orientation to light coming from above, the paired lateral areas being evolved primarily in relation to orientation in the horizontal plane. The analogy, however, is by no means proved or even clear, and the danger of phylogenetic deductions in such a case is obvious ^ ; in Froriep's (1906) view a common ancestry is more probable than a sequential derivation. A further hypothesis, the placode theory, usvially credited to von Kvipffer (1894), was suggested by Nuel (1887) and supported by Beraneck (1890), Burckhardt (1902) and Lubosch (1909). It postulated the development of ectodermal placodes homologous with the lateral line organs from the anterior members of which the olfactory organs, the membranous labyrinth of the ear and the Jens of the lateral eyes were developed. The lens was originally vesicular and was considered to form an eye with a verted retina ; the definitive retina emerged from the central nervous system to act as its optic ganglion, homologous with a spinal ganglion, and eventually as phylogenetic evolution proceeded, took over the sensory function of the lens which degenerated into a dioptric accessory. This theory, however, has long been in disrepute since no evidence, ontogenetic or phylogenetic, connects a non-sensory retina with a sensory lens. The origin of the lens^ — the other major factor in the development of the vertebrate eye — has also given rise to speculation. The homologous position of the olfactory and otic anlages suggested first to Sharp (1885) that this structure arose from an ectodermal placode and was in its own right a sensory structure. Without attributing photo- sensitive properties to its cells as called for in the preceding theory of retinal development, several investigators have been attracted to the view that the lens is an independent organ derived from an anterior placode of the epibranchial series (Jelgersma, 1906 ; Studnicka, 1918 ; Schimkewitsch, 1921). The evidence of experimental embryology is conflicting. Many experimenters have established that the presence of the optic vesicle is necessary for the development of the lens, and some liave claimed that this structure alone is sufficient for its deter- mination so that a lens will form from undifferentiated ectoderm at an abnormal site if the optic cup is transplanted thereto. Others have 1 Seo -vritings of Balfour (1878-81), Metcalf (1906), Keibel (1906), Buxton (1912), Bti ; 921), and others. THE VERTEBRATE EYE 247 found that a lens may partially or completely develop if the retinal anlage has been removed from the optic plate at an early stage or in anencephalic monsters.^ It may well be that there is some tendency for the formation of a lens inherent in the ectoderm of the region where it is normally found ; but on the whole, in the present stage of our knowledge, the evidence would seem to suggest that this structure is secondarily formed, called into existence normally by two mutually reinforcing inductors — the cells of the optic vesicle and the mesoderm of the head — although in certain experimental conditions no further stimulus beyond that provided by the latter may be necessary (Twitty, 1930-55 ; Woerdeman, 1950 ; Liedke, 1951). It would seem, therefore, that despite the considerable amount of thought expended on the question, the emergence of the vertebrate eye with its inverted retina of neural origm and its elaborate dioptric mechanism derived from the surface ectoderm, is a problem as yet unsolved. Indeed, appearing as it does fully formed in the most primitive species extant today, and in the absence of transition forms with which it can be associated unless by speculative hypotheses with little factual foundation, there seems little likelihood of finding a satisfying and pragmatic solution to the puzzle presented by its evolutionary development. Balfour. J. Anat. Physiol., 9, 128, 408 (1878). A Treatise on Comparative Embryology, London (1881). Beckwith. J. e.rp. ZooL, 49, 217 (1927). Benoit. Bull. Biol. France Belgique, 71, 393 (1937). Beraneck. Arch. Sci. phys. nat., Geneve, 24, 361 (1890). Boveri. Zool. Jb., Suppl. 7, 409 (1904). Biitschli. Vorlesiingen it. vergl. Anat., Berlin (1921). Burckhardt. Verh. int. Zoologencotig. (1901), 621 (1902). Buxton. Arch, vergl. Ophthal., 2, 405 (1912). Choi. Folia anat. japon., 10, 29 (1932). Dohrn. Mitt. zool. Stat. J^eajoel, 6, 432 (1885). Estable. Ayx. Inst. Neurol., Montevideo, 1, 328 (1927). Franz. Bolk's Hb. d. vergl. Anat. d. Wirbeltiere, Berlin, 2 (ii), 989 (1934). von Frisch. Pfli'igers Arch. ges. Physiol., 138, 319 (1911). Froriep. Hertwig'a Handbnch d. vergl. und exper. Entwicklungslehre d. Wirbel- tiere, Jena, 2 (1906). Anat. Anz. 29, 145 (1906). Hagedoorn. Arch. Ophthal. (Chicago), 16, 783 (1936). Hescheler and Boveri. Vjschr. naturf. Ges. Zurich, 68, 398 (1923). Jelgersma. Morphol. Jb., 35, 377 (1906). Keibel. Klin. Mbl. Augenheilk., 44 (2), 112 (1906). von Kennel. Diss., Dorpat (1881). Krause, W. Arch. mikr. Anat., 11, 216 (1875) ; 12, 742 (1876). von Kupffer. Studien zur vergl. Entwick- lungsgeschichte d. Kopfes d. Kranioten : II. Die Entwicklung d. Kopfes v. Ammocoetes planeri, Munich (1894). Lange. Zbl. prakt. Augenheilk., 32, 131 (1908). Lankester. Darwinisyn and Partheno- genesis, London (1880). Quart. .J. micr. Sci., 31, 445 (1890). Leboucq. Arch. Anat. micr., 10, 555 (1909). Leplat. C. B. Ass. Anat., 17, 194 (1922). Lewis. At)ier. J. Anat., 3, 505 (1904). Liedke. J. exp. Zool., 117, 573 (1951). Lubosch. Morphol. Jb., 39, 146 (1909). Mangold. Ergebn. Biol., 7, 193 (1931). Metcalf. .4/ia^ .4h;., 29, 526 (1906). Miiller, W. Beit, zur Anat. unci Physiol. {Festgabe C. Eudwig), Leipzig, 2 (1875). Nowikoff. .4cac/. Tcheque d. Sci., Bull. internat. Clin. d. Sci. math., nat. med., 33, 131 (1932). » See Lewis (1904), Keibel, (1906), Srockard (1910), Spemann (1912), Leplat (1923), Beckwith (1927), Mangold (1931), Choi 1932), Waddington and Cohen (1936). 248 THE EYE IN EVOLUTION Nowikoff. Biol. Zbl., 52, 548 (1932). Z. Morphol. Oekol. Tiere, 29, 374 (1934). Nuel. Arch. Biol., Gand, 7, 389 (1887). Parker. Amer. Nat., 42, 601 (1908). Amer. J. Physiol., 25, 77 (1909). Scharrer. Z. vergl. Physiol., 7, 1 (1928). Schimkewitsch. Lehrbuch d. vergl. Anat. d. WirbeUiere, Stuttgart (1921). Schwalbe. Graefe-Saemisch Handbuch d. ges. Augenhk., Leipzig, 1, 398 (1874). Sharp. Proc. Acad. Nat. Sci. (Phila.), 300 (1885). Sleggs. Amer. Nat., 60, 560 (1926). Spemann. Zool. Jb., Abt. Zool. Physiol., 32, 1 (1912). Stockard. Avier. J. (1910). Anat., 10, 369, 393 Studnicka. Anat. Anz., 41, 561 (1912); 44, 273 (1913). Zool. Jb., Abt. Anat., 40, 1 (1918). Tretjakoff. Z. wiss. Zool., 105, 537 (1913). Twitty. J. exp. Zool., 55, 43 (1930). In Analysis of Development. Phila., p. 404 (1955). Waddington and Cohen. J . exp. Biol., 13, 219 (1936). Walls. Arch. Ophthal. (Chicago), 22, 452 (1939). Willmer. Symposia Soc. exp. Biol., 7, 377 (1953). Woerdeman. Aim. Biol., 26, 699 (1950)- Young. J. exp. Biol., 12, 254 (1935). THE GENERAL STRUCTURE OF THE VERTEBRATE EYE We have seen that the eyes of Vertebrates are very true to type and (apart from a few degenerate forms ^) consist essentially of a retina derived from neural ectoderm, a lens derived from the surface ectoderm, a uvea wit/h a nutritive function, a protective tunic the anterior segment of which is transparent, and a dark chamber filled with the vitreous body, the entire organ being encased in the orbital cavity and moved by a group of extra-ocular muscles. All the varia- tions in structure — and they are marked and of great interest — seen in the major classes within the phylum are incidental in nature and have evolved essentially as adaptations to differences in habitat or function. Of all the ocular tissues the retina is, of course, the most important and undoubtedly the most interesting. Apart from the abundance and motility of its pigment, its occasional assumption of a tapetal function and the rare presence of oil-droplets, the pigmented epithelium shows little fundamental variation. The retina proper (the pars optica retinae) regularly comprises three layers of cells arranged in the following strata (Fig. 263) : NEURONE I (percipient elements) NEURONE II (conductive and associa- tive elements) NEURONE III (conductive elements) '1. Layer of rods and cones. 2. Outer nuclear layer. >3. Outer plexiform layer. 4. Inner nuclear layer (bipolar, horizontal and amacrine cells). >5. Inner plexiform layer. 6. Ganglion cell layer. 7. Nerve fibre layer. The sustentacular functions of the glial cells of the central nervous system are taken over by large fibres of Mtiller, the nuclei of which lie in the inner nuclear layer, while their extremities combine to form an 1 p. 721. THE VERTEBRATE EYE 249 external limiting membrane between the rods and cones and their nuclei and an internal limiting membrane on the inner surface of the nerve-fibre layer. Throughout the vertebrate phylum the structure of the retina is remarkably constant, the layers varying only in the M> «=^ «ai • ^* Nomina vitrea ^ "4i» (^ **niqmenf epithelium V I' Fig. 263.— The Humax Retina. At the left, the retina in the nasal fundus as it appears after fixation in Kolmer's fluid, nitro-cellulose embedding, ]\Iallory's trij^le stain or Heiden- hain's haematoxylin and phloxine. At the right, the neuronic hook-up of the retina, with examples of its principal elements, as revealed by the Golgi methods ( X .500) (Gordon Walls, based largely on the work of Polyak, 1941). o, amacrine cell (diffuse type) ; h, bipolar cells of ordinarj^ "midget" type; c, cones; ch, "centrifugal" bipolar (believed to conduct outward through the retina rather than inward) ; dh, diffuse bipolar cells, connecting with many visual cells, chiefly rods ; g, ganglion cells of ordinary " midget " type ; /;, horizontal cell with dendrites connecting only with cones, axon with both rods and cones at some distance; m, Miiller's fibre (forms limiting mem- branes) ; pg, " parasol" ganglion cell (one of .several giant types, connecting with many bipolars) ; r, rods. regularity of their architecture and in the density and relative pre- ponderance of their cellular elements ; even in Cyclostomes the typical layering can be recognized although the various elements tend to be intermingled, particularly the ganglion cells \\-ith the inner nuclear layer. These minor variations which occur will be noted in the subsequent chapters. 250 THE EYE IN EVOLUTION THE VISUAL CELLS Constitute the most important and interesting of the constituent elements of the retina. i They have been divided into two types — rods and cones (Figs. 264-267). Typically the rod consists of an outer and inner segment, a nucleus and a foot -piece. The outer segment, possibly representing the cilium of the ancestral Fig. 264. Fig. 266. Figs. 264 and 265. — Typical Rods and Cones of the Fbog, Baxa pipiess (Gordon Walls). Fig. 264. — (a) A common rod (dark- adapted) ; (6) a green rod. Fig. 265. — A typical cone (dark- adapted). d, oil-droplet ; e, ellipsoid ; /, foot- piece ; I, external limiting membrane ; m, myoid ; n, nucleus ; o, outer segment. Fig. 267. Figs. 266 and 267. — Typical Rods and Cones of Man (after Greeff). Fig. 266. — A typical rod. Fig. 267. — (a) A peripheral cone near the ora ; (6) a peripheral cone near the equator ; (c) a macular cone. o, outer segment ; 6, inner segment ; c, cell fibre ; d, cell nucleus ; e, cell foot ; /, ellipsoid ; g, myoid. ependymal cell, is the photosensitive tip of the cell ; the inner segment, possibly representing the columnar body of the ependymal cell, has at its outer end an ellipsoid containing mitochondria, presumably the principal site of metabolic activity, while its inner end is termed the myoid ....hough it is by no means always contractile. The cone has ^ For structure of rods and cones, see C. Miiller (1926), Wislocki and Sidman (1954), Sidman and Wislocki (1954) (histochemistry) ; Sjostrand (1949-53), de Robertis (1956) (ele( -n-microscopy) ; Saxen (1955-6) (development) ; Sidman (1957) (phase- contrast ail fractometry). THE VERTEBRATE EYE 261 the same component parts, the outer segment being typically (but not invariably) conical, the inner segment typically fatter, shorter and more squat than the corresponding part of the rod, often with an oil- droplet in the ellipsoid, and sometimes with a paraboloid composed of glycogen lying more proximally ; the nucleus is relatively larger and the foot-piece more widely spread. Variations to this standard structure are common, such as the presence or absence of oil-droplets, the occurrence of double, triple or even quadruple elements, and so on ; these will be discussed in the sections on systematic anatomy. While these are the typical structural features, however, the variations in the morphology of the rods and cones are so marked as to have led to much confusion and some controversy ; some rods resemble cones more closely than some members of their owii family, while the cones of a well-developed fovea often resemble elongated rods more closely than typical cones (Fig. 267c). Indeed, in our systematic survey we shall on more than one occasion run up against difficulties in describing particular visual cells either as a rod or a cone. Schultze (1866), who first clearly differentiated the two types of cell, did so primarily on anatomical grounds, his three criteria being — (o) the cylindrical termination of the rods in contrast to the conical tip of the cones, (b) the more external position of the cone-nuclei close to the limiting membrane owing to the shortness of the inner segment, and (c) the knob-like ending of the rods in contrast to the spread-out foot-piece of the cones. Unfortunately, all these conditions ai'e violated, sometimes even in the same retina. The tip of the cone may be slender, elongated and cylindrical (as in lizards and birds, Verrier, 1935 ; Detwiler, 1943) ; the nuclei may lie in a single layer (amphibians, Saxen, 1953), or the usual arrangement may be rev^ersed (some fishes and amphibians : Cajal, 1893 ; Franz, 1913 ; Memier, 1929) ; while the foot-pieces of rods may be branched (some fishes, amphibians and birds: Greeff, 1900; Putter, 1912; Detwiler, 1943). Differential methods of staining have been attempted as a criterion (Dogiel, 1888 ; Kolmer, 1936 ; Wolff, 1949 ; Wislocki and Sidman, 1952 ; Saxen, 1953 ; and others) and again have led to inconclusive results. A further point of differentiation is a study of the connections of the visual cells ; several rods are typically associated with one bipolar cell, while each foveal cone is ordinarily connected with one bijoolar cell ; but again, this relationship is not maintained by the peripheral cones nor in retinae without a fovea. It is possible that, when more fully developed, the study of the ultra-microscopic structure may provide further evidence whereon a distinction between the two types of cell may be based. The difficulty in anatomical differentiation has naturally stimulated attempts at a functional basis for classification, for it is generally conceded that the cones mediate photopic (and colour) vision while the rods are concerned with scotopic vision. Tlie physiological distinc- tion between " photocytes " and " scotocytes,"" however, is equally fraught with difficulties. The presence of rhodopsin or its relatives would theoretically substantiate ihe presence of rods, but while this is 252 THE EYE IN EVOLUTION possible in a uniform retina by extraction of the photopigments, the method is inapphcable in a duplex retina since the concentration of pigment is not sufficiently great to allow the histological demonstration of vitamin A even by methods so delicate as fluorescence -microscopy (Stern, 1905 ; Hopkins, 1927 ; Walls, 1935 ; Stenius, 1940 ; Greenberg and Popper, 1941 ; see Saxen, 1954 ; and others). There is no doubt, of course, that fundamentally the two elements are alike and it is obvious that within the vertebrate phylum many transitional forms between the two exist ; between these, wherein the anatomical difficulties of differentiation occur, a sharp distinction may be illegitimate. Both are probably derived from the same primitive ancestral cells, and it has been suggested that cones are transformed into rods during development (Steinlin, 1868 ; Bernard, 1900-3 ; Cameron, 1911), a theory, however, which later evidence has questioned (Detwiler, 1943 ; Birukow, 1949 ; Saxen, 1954) ; similar criticism has been directed to the theory of Walls (1934) that the one may be transmuted into the other in phylogeny. Walls's theory — ingenious, attractive, fanciful and mvich criticized — is that the primitive visual cell of Vertebrates was a cone and that therefrom rods were evolved as a transmvitation-form with a view to increasing sensitivity with the development of rhodopsin — presumably first in deep-sea types. The brilliance of illumination on land allowed many reptiles (diurnal lizards) to retain a pure- cone retina ; their adoption of nocturnality as a protective measure forced some species (Xavtusia) to develop a transitional rod-like element, and the adoption of complete nocturnality by most geckos led to the transmutation into rods. The visual elements of many snakes are similarly interpreted, the cones of some secretive nocturnal types showing a structvnal or a complete transmutation into rods, in the first case withovit, in the second with rhodopsin. It is interesting that recent research has to a considerable extent confirmed this somewhat revolutionary view. That such a trans- mutation had in fact occurred is suggested by the finding of Crozier and Wolf (1939^ that the rod-retina of the gecko, Sphcerodactylus, has a critical fusion frequency similar to that obtained in the turtle with its predominantly pure-cone retina. The same conclusions could be said to follow the finding of Underwood (1951) that some primitive Jamaican geckos had oil-droplets in their rod-like receptors. The peculiar pigment with its unusual absorption curve for a substance based on vitamin A^ (maximum at 524 m^ti) described in certain geckos by Denton (1953) {Gekko gekko) and Crescitelli (1956) {Phyl- lurus) again could perhaps be interpreted as an attempt to transform ancestral cones into rods, as if they were unable to re-invent rhodopsin for lack of the suitable protein, and had thus been forced to conjugate their ret;;,enei as a chromophore and produce a pigment with an absorpti intermediate in spectral position between those generally THE VERTEBRATE EYE 253 accepted as typical of rod-pigments and cone-pigments. Finally, the observations of Bellairs and Underwood (1951) support the view that snakes were derived from burrowing lizard-like ancestors. In the present state of our knowledge the problem, which raises questions as difficult as they are interesting, is unsolved. Combinations of these visual elements are frequently encountered in several classes of the vertebrate phylum. Double rods are rare (geckos and some nocturnal snakes). A second rarity is the twin cones — a fusion of identical elements — which are found only in Teleo- steans (Figs. 347-8). Double cones are more common, appearing first in Holosteans and occurring in every other class. ^ Typically they represent the fusion of two unlike elements, the principal resembling the single cones in the same retina and the accessory, generally of a simpler type, rarely containing an oil-droplet but frequently an unusually large paraboloid. In Amphibians, Saxen (1954-56) has brought forward evidence that the double visual elements represent not the fusion of two cones as has generally been thought but the fusion of a rod with a cone. Triple " cones " (perhaps two cone-like com- ponents with a third rod-like component, Saxen, 1953) occur in some Teleosts (trout) and Anurans, while quadruple elements have also been described in the minnow, Phoxinus (Lyall, 1956).- The origin of these double cells has given rise to some controversy. The sceptical view that they were histological artefacts was put forward by Koganei (1884) and has been maintained by such writers as Cameron (1911) and Roze- meyer and Stolte (1930). There seems no doubt, however, that they do exist. Dobrowolsky (1871) put forward the hypothesis that they resulted from the incomplete division of single cones, a view upheld by Howard (1908) and Franz (1913). On the other hand, Detwiler and Laurens (1921), finding that double cones appeared during development at a stage when no further cell-divisions took place, suggested that they were produced by the fusion of two separate progenitors ; this view has been well substantiated in Amphibians by Saxen (1954-56). The physiological significance of the association of more than one visual cell is not understood. The fact that the dendrites of the two components sink to different depths in the outer plexiform layer suggests some difference in func- tion (Cajal, 1893 ; Greeff, 1898), while the observation of v. Genderen-Stort (1887) that photomechanical reactions are confined to the principal elements points to the probability that the accessory element has a subsidiary function. Whether this is visual or metabolic, the two elements living in symbiosis (Howard, 1908 ; Franz, 1913), is conjectural. Apart from the fundamental structure of the retina the other ocular tissues, although in general conforming to the vertebrate plan seen in man (Fig. 268), show considerable variations depending upon ^ Many Teleosts, Protopterus, Amjjhibians, Reptiles except some snakes, Birds, the platypus, and Marsupials. 2 See also footnote, p, 364. 254 THE EYE IN EVOLUTION an unusually wide range of adaptive demands, for vertebrates have succeeded in making themselves at home in every environment where life is possible. These differences have been very considerable and the adaptations demanded have been great. The vertebrate eye was initially evolved for vision in shallow water ; it has been asked to adapt itself for vision in the abyss, in the rivers, in the mud of the swamps, on land and in the air, and on occasion to readapt itself for Fig. 268. — Diagram of the Longitudinal Section of the Human Eyeball. a, angle of anterior chamber. ac, anterior chamber. aCV, anterior ciliary vessel. C, cornea. CB, ciliary body. Ch, choroid. CO, ocular conjunctiva. CS, canal of Schlemm. DS, dural sheath. F, fovea. I, iris. L, lens. ON, optic nerve. OS, ora serrata. PC, posterior chamber. PCV, posterior ciliary vessel. PP, pars plana. R, i-etina. RM. rectus muscle. S, sclera. SCT, subconjunctival tissue. V, vitreous. VS, vaginal sheath. VV, vortex vein. Z, zonule. vision in the seas ; it has been asked to fit itself for vision at night, in twilight or in dark cavernicolous surroundings and in the brightest of dajdight ; it has been asked to cater for panoramic vision where the detection of movement is paramount, or to accommodate itself to the finest stereoscopic prowess, to meet the needs of a sluggish or an active habit (ji Jife, to be content with a vague apperception or to evolve the capacit\ for minute resolution in form vision and master the intricacies of colou, iiion. All this — and more — it has done ; and in so doing it has trit-i, and often discarded, now this expedient, now that. THE VERTEBRATE EYE 255 The requirements of aerial vision when Amphibians left the water for the dry land were met by an optical reorientation of the primitive aquatic eye to suit the new medium and the provision of lids equipped with elaborate glandular structures as a protection against drying ; a return to water (as in the whale or the dolphin) has led to a reversion of this process. The requirements of an amphibious life have resulted in the adoption of a host of ingenious devices to allow an easy transition from one medium to the other and to maintain adequate vision in each. The dangers of a burrowing habit or a sandy environment have led to the acquirement of protective " spectacles " (in lizards and snakes). The vagaries of nocturnal, crepuscular or diurnal vision are met by several expedients — variations in the size of the eye and the lens, in the relative proportions of the percipient elements in the duplex retina, in the size, shape and motility of the pupil, and the provision of a tapetum or argentea, choroidal or retinal in site, fibrous, cellular or crystalline in nature, which augments a scanty supply of light by its mirror-like effect. The requirements of acuity of vision are met by the development of an area centralis and a fovea, the receptor elements of which are provided with individual nervous connections ; stereopsis by the provision of more than one fovea or by a swinging forward of the visual axes ; focusing at varying distances by a host of accommoda- tive devices — the development of accessory retinae close to the dioptric apparatus (as in the tubular eyes of deep-sea fishes), variations in the position of the visual cells relative to the lens (as in some bats or in the horse), the use of a stenopoeic pupil (as in the gecko or the cat), the deformation of the eye by muscular action from outside (as in the lamprey), the pushing or pulling of the lens backwards or forwards (as in some Fishes, Amphibians and snakes), or a change in its shape by squeezing it (as in Reptiles and Birds) or relaxing it (as in Mammals). These serve to illustrate the multitude of expedients adopted by an organ of unique plasticity to meet the requirements of environments so completely different as the abyss of the ocean and the upper air, or habits so diverse as the sluggishness of a parasite and the activity of a bird-of-prey. The general scheme of phylogenetic development of the vertebrate eye is therefore interesting in that it does not show a steady and gradual increase in efficiency, but illustrates the elaboration of more than one type from a common beginning along different lines to reach more than one culminating point. The common beginning may be found in Cyclostomes, the eyes of which are primitive and show no specializations. From this starting point three peak-points have evolved in types which in their habits of life are peculiarly visually conscious — in teleostean Fishes, Sauropsida (lizards and Birds) reaching its highest development in Avians, and among Mammals in 256 THE EYE IN EVOLUTION the Primates. In these three groups alone is a fovea found making possible a good acuity of vision ; in these, highly developed accommo- dative mechanisms are present allowing accuracy of form vision over a wide range of distances ; and in these alone good colour vision has been demonstrated. In each of these the optic axes may be swung forwards so that the visual fields are made to overlap, thus rendering it possible for binocular to replace panoramic vision ; in the last group a partial decussation of the optic nerve fibres allows an anatomical basis for the coordination of ocular movements ; and finally, a neo- pallium built up upon the sense of vision replaces the original archi- pallium which was based upon the sense of smell. In this way the dyscritic mechanism of the simple eye of the lower Vertebrates, which was essentially adapted to the biologically primitive function of the appreciation of light and movement, developed the capacity for the intelligent appreciation of complex visual patterns and the potentiality to form reasoned visual judgements. The interesting thing is that the eye of each of these types has developed separately and independently ; between them there is no evolutionary sequence, for all have attained their high degree of efficiency by different expedients which, when they show affinities, owe their relationship to the fact that they have evolved not the one from the other, but all from the same original substrate of physiological potentialities. It is also interesting that of these types the sauropsidan eye is the most efficient as an optical mechanism ; of all the three, Birds have relatively the largest and absolutely the most specialized eyes, tlie most efficient focusing apparatus, a pecten structure instead of a retinal system of vessels, the most complex macular arrangements, and the highest visual acuity. The eye of man cannot therefore be considered as representing the acme of efficiency as an optical instru- ment ; it is to the unique and transcendent development of the associated cerebral centres that it owes its functional predominance. Bellairs and Underwood. Biol. Rev., 26, Dobrowolsky. Arch. Anat. Physiol., 208 193 (1951). (1871) Bernard. Quart. J. micr. Sci., 43, 23 Dogiel. Anat. Anz., S, 133 {li (1900) ; 44, 443 (1901) ; 46, 25 Franz. Oppel's Lhb. vergl. mikr. Anat. (1903). Wirbeltiere, Jena, 7, 1 (1913). ^''■''n°,r^o. ^- '"'■^^- ^''^■"'°^" 31' ^'" van Genderen-Stort. v. Graefes Arch. Ophthal., 33 (3), 229 (1887). (1949). Cajal. LaCe//!/7e, 9, 119 (1893). r^ «• ^ e> , , r>, • , la i«i Cameron. J. Anat. Physiol. ^6, 45 {\9\l). ^''^^f^oo.f- ^'''^'^'°^- ^'^i/*'°'- 16' ^^^ Crescitelli. J. gen. Physiol., ^0,217 {1956). GraehSaemisch Hb aes Auaenheilk Crozier and Wolf. J. gen. Physiol., 22, fr^ V !^ naf^'a^^ Augenheitk., 555 (1939) ' ' ^'^P- '^ (iJUU). Denton. XIX Internal. Cong. Physiol., ^'^''^iT^ f?*?,^°PP'''"- ^"^'^er. J. Physiol., Abstr. Communications, 306 (1953). ^34, 114 (1941). Detwiler. Vertebrate Photoreceptors, N.Y. Hopkins. Z. vergl. Physiol., 6, 345 (1927). (1943) Howard. J. Morphol., 19, 561 (190S). Detwiler an ; Laurens. J. comp. Neurol., Koganei. Arch. mikr. Anat., 23, 335 33, 493 (1921). (1884). THE VERTEBPvATE EYE 257 Kolmer. Mollendorff's Hh. niikr. Annt. d. Menschen, 3 (2). 310 (1936). Lyall. Nature (Lond.), 177, 1086 (1956). Menner. Z. vergl. Phy.sioL. 8, 761 (1929). MuUer, C. Z. Anat. Enlwick. Ges., 81, 220 (1926). Putter. Graefe-Saemisch Hb. ges. Augen- heilk.. III. 1, Kap. 10, 1 (1912). de Robertis. J. biophys. biochem. Cytol., 2, 319 ; suppL, 209 (1956). Rozemeyer and Stolte. Z. niikr. Anat. Forsch., 23, 98 (1930). Saxen. Ajin. Med. e.vp. Biol. Fenn.. 31, 254 (1953). Ann. Acad. Sci.fen. A IV, 23, 1 (1954). Acta Anat., Basel, 25, 319 (1955). J. Embryol. exp. Morphol., 4, 57 (1956). Schultze. Arch, niikr. Anat., 2, 175 (1866) ; 3, 215 (1867). Sidman. J. biophys. biochem. Cytol.. 3, 15 (1957). Sidniau and Wislocki. ./. histo-chem. Cytochem., 2, 413 (1954). Sjostrand. J. cell. comp. Physiol., 33, 383 (1949) ; 42, 15, 45 (1953). Steinlin. Arch. mikr. Anat., 4, 10 (1868). Stenius. Acta Physiol. Scand., 1, 380 (1940). Stern, v. Graefes Arch. Ophthal., 61, 561 (1905). Underwood. Nature (Land.), 167, 183 (1951). Verrier. Bull. Biol. France Belg., Suppl. 20, 1 (1935). Walls. Anier. J. Ophthal., 17, 892 (1934). Brit. J. Ophthal., 19, 129 (1935). The Vertebrate Eye, Michigan (1942). Wislocki and Sidman. Anat. Bee, 113, 540 (1952). J. conip. Neurol, 101, 53 (1954). Wolff. The Anatomy of the Eye and the Orbit, London (1949). 258 THE EYE IN EVOLUTION Fig. 269. — U. W. SoEMMP:RRiN(i (1793-1871). CHAPTER X THE EYES OF CYCLOSTOMES Although he made a classical description of the eyes of all classes of Vertebrates except Cyclostomes, I am introducing this chapter which is the first of a series dealing with the structure of the eyes of Vertebrates with the portrait of detmar wilhelm soemmerring (1793-1871) (Fig. 269) in view of the fact that he was one of the earliest writers to make a systematic study of this subject. It is true that many incidental observations had been made on the fijier structure of the eyes of different Vertebrates by such investigators as van Leeuwenhoek,^ Zinn ^ and Young,^ while compendia had been published by such authors as Bluraenbach,* Albers,^ and Cuvier ® ; but none is so delightful to read as is the thesis written in Latin which brought Soemmerring his doctorate in Gottingen in 1816, and was published in 1818 under the title De oculorum hominis animaliumque sectione horizontali commentatio ; the illustrations are so beautiful that several of them have been reproduced in the following chapters. D. W. Soemmerring, the son of an equally distinguished German ophtha,lmologist, S. T. von Soemmerring (who, it will be remembered, first described the macula lutea as a hole in the retina), was born in Frankfurt where in later life he practised for many years and where his jubilee as a doctor was officially celebrated in 1866. He is also remembered ophthalmologically for two particular observations — a description of the organic changes in the eye after the operation for cataract in which he described the annular remnant of the lens now universally known as Soemmerring's ring (1828), and the first description of a living cysticercus in the human eye (1830). The CYCLOSTOMES (kJk/\o9. round ; otoixx, a mouth), so called because of their round, jawless, suctorial mouths which differentiate them from all other Vertebrates, are the only surviving representatives of the large class of agnatha (a, privative ; yvddos, jaw) which flourished in great variety and numbers during Palaeozoic times and are now with this exception extinct. They are freely-swimming worm -like " pre-fishes "' of extreme antiquity, essentially primitive in their structure and differing in many ways from true Fishes, principally in the absence of jaws, by the single olfactory organ and by the absence of paired fins. Today they are represented by two existing types and a few others like them — the hagfishes (slime-eels) and the lampreys. The eyes of the former, buried deeply within the skm, are degenerate and sightless and are described at a later stage^ ; those of the latter, at first buried and later coming to the surface, constitute the most ' Epistolce physiologicce, Delphis, 1719. - Comment. Soc. Sci., Gottingen, 1754. 3 Philos. Trans., 1793. * Vergl. Anat., 1784. 5 Beyt. z. Anat. u. Physiol, d. Thiere, 1802. * Leg-ons d'anat. comparee, Paris, 1805. ' p. 734. 259 260 THE EYE IN EVOLUTION primitive type of vertebrate eye showing characteristics differing markedly from those of Fishes. THE LAMPREYS (PETROMYZONIDiE) The lampreys are large eel -like creatures found mainly in the seas and rivers of the northern hemisphere ; the sea lamprey {Petromyzon marinus), about 3 feet in length, and the fresh-water river lampern {Lanipetra fluviatilis), about 2 feet in length, eat worms and small crustaceans and are also ectoparasites on living fishes to which they attach themselves and feed by rasping off the flesh. From the latter species smaller brook lamperns (sand-prides) have presumably been derived ; these do all their feeding as larvae and after metamorphosis to the advilt form, breed and then die. Related genera are Mordacia and Oeotria from the coasts of Chile and Australasia, and Ichthyomyzon from the western coasts of North America (Fig. 270). The hfe-cycle of the lamjDrey is interesting and complex. The larva, or Ammocoetes (sometimes known as the " pride " when it was Fig. 270. — The Sea Lamprey, Petromtzon maris us. There are two unpaired median fins and a relatively large eye ; behind the eye are seven point-like gill-slits. For the head of the lamprey, see Fig. 862. thought to be a different species), is a small creature without a sucking mouth and with a solid spinal cord in which a medullary cavity subsequently develops ^ ; the eyes are extremely rudimentary and lie beneath the skin. Before metamorphosis the larva burrows in mud and the non-functional eyes are covered with opaque integument. At metamorphosis during the latter half of July, at the age of 2 to 4 years, great changes occur as the ammocoetes leaves the mud or sand and transforms into the eel-like adult, changes which include the develop- ment and emergence of the eyes. The simple and relatively undiffe- rentiated retina of the larva (retina A) rapidly becomes transformed into the functional adult tissue (retina B) and as it does so the over- lying skin atrophies and becomes transparent. The adult organ is rapidly formed, neither regressive, atrophied nor degenerate in type, but primitive in nature and embryonic in certain characteristics, particularly in the structure of the optic nerve. It nteresting that the animal also possesses pineal and parietal " eyes," a subjf ich will be fully discussed in a later chapter. ^ ' Compare p. 239, footnote. ^ p. 711. CYCLOSTOMES 261 THE AMMOCCETE EYE Since the original description by W. Miiller (1875), several studies have been made of the animocoete eye. The youngest specimen described was that of Ida Mann (1928) who figured a simple optic vesicle evaginated from the anterior cerebral vesicle lying close underneath the surface ectoderm (Fig. 271). At this early stage there was neither vitreous nor lens, the outer layer of the vesicle mM^m Fig. 271. — Section Through the Eye of the Ammoccetes (the Larva OF PETROMYZOy FLUVIATlLIs). There is neither vitreous nor lens ; the optic cup is closely folded upon itself, the outer layer being pigmented and the inner showing a considerable degree of differentiation. a, surface epithelium of the head ; 6, pigmented outer layer of the optic cup ; c, nuclei of the visual cells ; d, nuclei of bipolar cells ; e, ganglion cells with nerve fibres arising from them ; /, visual cells ; g, muscle mass of head ; h, optic nerve (Ida Mann). being pigmented and the inner showing differentiation into the three layers of cells characteristic of the vertebrate visual retina — visual cells (indistinguishable either as rods or cones), bipolar cells and gan- glion cells the axons of which constitute the oj^tic nerve. In somewhat older larvae (5-10 mm.), von Kupffer (1894) and Studnicka (1912) des- cribed a lens vesicle lying underneath the single layered ectoderm and completely separate from the ojjtic vesicle (Figs. 272 and 273), while Carriere (1885) in a more mature larva (30 mm.) described a lens, at this stage still vesicular, invagiTiated within the optic vesicle. Eventually the lens becomes solid, tlie anterior and vitreous 262 THE EYE IN EVOLUTION Figs. 272 and 273. — The Ammocoete Eye (after Studnicka). Fig. 272. — The eye of the 8 mm. lar\a of Pctromyzon, showing the optic vesicle and the smaller lens vesicle superficial to it. Fig. 273. — The eye of the 18 nun. ammocoetes showing the lens vesicle incor^jorated into the optic vesicle. In the latter the outer pigmented layer and the highly differentiated inner layer with the projecting visual cells are evident. chambers till ^\'\i\\ fibrillar material, the cornea is entirely cellular, the retina becomes relatively differentiated but blood vessels and mesodermal elements do not invade the vesicular eye (Mawas and Magitot, 1912; Diicker, 1924) (Figs. 274 and 275). Meantime the eye sinks beneath the skin to become separated from it by a considerable thickness of tissue. The depth at which the vesicular eye lies at this stage beneath the skin suggested to Hagcdoorn (1930) that the lens was derived from the retinal Fig. 274. — The Eye of the Ammoccetes. A\ a late stage. On top is the surface epithelium, underneath which lies the ii'i^sodernaal skin. Underneath this is the scleral cornea. The lens is fully ' vnied, as also are the anterior and vitreous chambers (a drawing from Mawas i CYCLOSTOMES 263 vesicle ; the suggestion that the eye of the lamprey differed from all other vertebrate eyes in that its elements were all autonomous in the sense that the entire oi'gan arose from the neural ectoderm is, however, by no means proven by the evidence submitted by this author and should be discarded. It is apposite that in the still more primitive eye of the myxinoid, Bdellost07na, Stockard (1907) found that the lens appeared in the usual vertebrate way as a vesicle from the surface epithelium inrlependently of the optic vesicle. LIGHT-SENSITIVE CELLS. In the ojiidermis of the tail of the animoccotes there are numerous iiiteresting cells cojiiously inncr\'ated from the lateral line. Morphologically they resemble the ajiolar visual cells seen in tlie earthworm or ¥ui s THiMncH THE l'irtebrates. the epithelial layers of the iris continue forwards the state of pigmentation of the corresponding retinal layers ; the anterior layer is pigmented, the posterior un- pigmented almost up to the pupillary border. The anterior surface of the iris has a light metallic sheen due to a fine argentea comprised of a layer of closely packed cells containing guanine crystals, a configura- tion which is not continued into the choroid. The angle of the anterior chamber is constructed on simple lines. A ring of large endothelial cells encircles the periphery of the cornea as the ANNULAR LIGAMENT, continues anteriorly with the corneal endothelium and sends strands posteriorly to the choroid suggestive of the tensor choroidese of Teleosteans ; while from the region of this ring, fine strands span the angle to reach the anterior surface of the iris, reminiscent of a pectinate ligament. The large and almost circular lens is wedged in the immobile pupil and approximates the cornea, separated from it at most by a capillary space ; it is held in place by the support of the cornea in front and the vitreous behind. The lens is primitive in formation compared with the structures found in other Vertebrates, showing a central zone of polygonal or rounded fibres and a somewhat irregular arrangement in the periphery without 1 The origin of the aqueous humour of Cyclostomes and Fishes is obscure, but it is possible that the ocular fluids are maintained directly by osmosis through the cornea, the pressure being ccjuilibrated through the blood-stream. In fresh-water fish and the lamprey the blood is hypertonic to the mediimi so that the body fluids are constantly replenished by the absorption of water through the skin by osmosis, the fish excreting the large cjuantities of fluid thus absorbed by producing immense quantities of urine. In marine teleosts, on the other hand, the blood is hypotonic to the sea-water ; dehydra- tion is avoided only by the copious drinking of the latter. This is actively absorbed in the gut against tlie osmotic gradient while the excess of salts is excreted differentially in the gut, kidneys and gills. Selachian fishes maintain a high level of urea in the blood (some 2%) thus keeping it at a higher osmotic level than sea-water ; the latter is thus absorbed osmotically while the excess of salts is excreted through the gills. It would appear that Myxine has a salt concentration in the blood approaching that of sea-water and thus higher than that of any other vertebrate (Robertson, 1957). It is probable that the fluid-exchange and the pressure ecjuilibrium in the eye is main- tained in much the same manner. There would seem to be no anatomical basis in any cyclostome or fish for an elaborate secretorj' mechanism for the intra-ocular fluid ; the only types which possess ciliary processes are the Selachians and these, in Franz's view (1934), probably serve merely as a mechanism for supporting the lens. All land animals, on the other hand, secrete the aqueous humour. It should not be considered strange that the tissues of the earliest Vertebrates (fresh-water agnathous fishes) were hj'pertonic to the medium in which they lived ; the same relationship is seen in the tissue-cells of inan which are maintained in a state of hypertonicity in com- parison with the surrounding tissue-fluid by an osmo- regulation depending on respira- tory activity (see Bartley, Davies ami Krebs, Proc. n-y. Soc. B., 142, 187, 1954). 268 THE EYE IN EVOLUTION sutures (Capraro, 1 934-37 ).i It has a light yellow coloration derived from a pigment the composition of which is unknown (Plate, 1924 ; Franz, 1932 ; Walls and Judd, 1933). The retina, even at this early stage of Vertebrate evolution, shows the essential architecture of the vertebrate eye ; but is entirely avas- cular and without any suggestion of an area centralis (Fig. 280). Next to the outer layer of pigmentary epithelium lie the visual elements, ^^=' M»»^-.^ Fig. 280. — The Retina of Lampetra fluviatilis. g, ganglion cells ; i, internal nuclear layer, consisting essentially of horizontal cells above and bipolar cells below ; e, external nuclear layer ; ?», visual cells ; p, pigmented epithelium (Feulgen, X 370) (Katharine Tansley). thereafter their nuclei form an outer nuclear layer which is followed by a combined layer containing bipolar cells, horizontal cells, amacrine cells and a few sparse ganglion cells. The nature of the visual elernejifs has given rise to some controversy, but most authorities are now agreed that even in this, the most primitive of Vertebrates, two types of cell exist, a relatively long and a relatively short cell, the former with a voluminous ellipsoid and short external segment, the latter with a smaller ellipsoid capped by a longer external segment. The differentiation between the two types and their relative numbers vary in different families (Walls, 1035). In the primitive 1 Compare the lens of lizards, p. 361. CYCLOSTOMEvS 269 genus, Ichthyomyzon, the two differ little in size ; in Lmnpefra fluviatilis the difference is marked and in Entosjjhenus it is maximal. In shallow- water forms such as Lampetra fluviatilis and the brook lampreys, the two types are found in apjaroximately equal numbers, while in those which live in deeper waters {Petromyzon marinus, etc.) and presumably demand greater sensitivity to light, the short greatly outnumber the long (Figs. 281 and 282). The existence of a duplex mechanism in the retina has not always been accepted and the nature of the cells has long been called in ciuestion. Heinrich Miiller (1857) who first studied the subject in L. fluviatilis, differentiated the Fig. 281. — The Visual Cells of the Atlantic Lamprey, PET/to.vrzoy MARIXVS. Showing the " long "' and the " short " elements ( X 1,000) (Gordon Walls). Fig. 282. — The Visual Cells of the New Zealand Lamprey, Geotria australia. There are three types of cell in apjDroximately equal numbers, one plump (to the left), one slender (to the right) and an intermediate type (middle) with a eosinophobic ellipsoid ( X 1,000) (Gordon Walls). two types of cell, and while initially he called them both cones, he later (1862) suggested that the short elements were rods. Since his time every possible suggestion has been made — that both cell-types are rods (Schultze, 1866-71 ; Franz, 1932) ; that both are cones (Kohl, 1892) ; that the cells are neither rods nor cones but primitive and undifferentiated in type (Plate, 1924 ; Diicker, 1924); that the long cells are cones and the short rods (Walls, 1935); or — the view of the majority of workers — that the long cell is a rod and the short a cone (W. Krause, 1868-76 ; Langerhans, 1873-76 ; Greeff, 1900 ; Tretjakoff, 1916 ; R. Krause, 1923). Most of the evidence brought forward in support of these divergent views is morphological in nature — a somewhat dangerous basis for the differentiation of rods and cones. ^ The demonstration by Kiihne (1878) that rhodopsin is present in the retina of the lamprey proves the presence of rods ; the difference in the two types of cell suggests strongly a duplex population; ' p. 251. 270 THE EYE IN EVOLUTION but the presence of a dendritic foot-piece in the long cells and a smooth knob in the short (Tretjakoff, 1916) as well as the comjoarative and taxonomic evidence collected by Walls (1935), provide weighty evidence in favour of Heinrich Midler's original suggestion that, desj^ite their length, the long elements are probably cones and the short, rods. At the present time, as was suggested by W. Miiller (1875) and maintained by Franz (1934), it may be safer, while admitting the presence of two morphologically different types of cell, to refrain from dogmatic differentiation until more conclusive evidence derived from their histochemistry or neural connections is available. The oj)tic nerve is primitive, consisting (unlike that of Fishes) of non-myehnated fibres (Briiesch and Arey, 1942) ; as occurs in the human embryo there is no septal system but merely an axial column Figs. 283 and 284. — The Optic Nerve of Cyclostomes. Fig. 28,3. — The optic nerve of the ammoeopte larva (after Studnicka). Fig 284. — The optic nerve of Lumpetra fluvintili.s (after Diicker). In both cases there is no sejital system but merely an axial column of ependymal cells running down the centre of the nerve sending processes radiating to the surface. d, dural sheath ; pa, pia arachnoid sheath ; n, nerve fibres ; e, epen- dymal cells sending out radiating processes ; oa, ophthalmic artery. of cell-bodies, probably ependymal in nature, running down the nerve, each sending processes radiating to the sm-face forming a primitive oligodendroglial system (Deyl, 1895 ; StMnicka, 1912 ; Keibel, 1928 ; Walls, 1942 ; Prince, 1955) (Figs. 283 and 284). The chiasma remains within the brain and in it the optic nerves cross as separate individuals without division into fascicles or bundles. THE EXTRA-OCULAR STRUCTURES of the eye of the lamprey are simple. Contrary to the configuration found in all other Vertebrates, there is no skeletal orbit, but the organ lies in a simple connective - tissue ca -de. The orbits and the eyes are laterally placed so that no CYCLOSTO:\IES 271 binocular field is possible. The rectus muscles are largely blended together and are inserted into the globe as a ring around the periphery of the cornea ; the inferior oblique arises in common with the internal rectus, and the superior oblique, identifiable only by its nerve-supply, is inserted into the infero-tem}Doral quadrant of the globe. The nerve- supply to the muscles corresponds to the scheme common to all Vertebrates (including man) except that the sixth cranial nerve appears to supply the inferior as well as the external rectus ; it may be, however, that the trunk contains fibres derived from the third nucleus. The most interesting feature, however, is the coknealis muscle, a Fig. 285. — The Cornealis Muscle of the Lamprey. The cornealis muscle, c, running horizontally outside the orbit on the caudal aspect of the globe, showing its insertion into the cornea (Mallory"s phospho-tungstic acid hsematoxylin) ( ; 44) (Katharine Tansley) (cf. Fig. 276). massive muscle arising outside the orbit on the caudal aspect and inserting into the transparent dermal cornea (Tretjakoff, 191G) (Fig. 285) ; its function is accommodative, dra\\ing this element of the cornea taut and, in so doing, flattening the scleral cornea, pressing the lens backw ards towards the retina and thus rendering the normally myopic eye {■ — 8 dioj^tres) ennnetropic or even hypermetropic. Unlike man, the lamprey thus accommodates for distant vision. ^ An accom- modative mechanism acting by deforming the globe from the outside is among Vertebrates unique to the lamprey. Bruesch and Arey. J. com p. Xeui-ol.. 77, 631 (1942). Capraro. Arch. ital. Anat. Embriol.. 32, 491 (1934) ; 38, 1 (1937). Monit. Zool. iluL, 45, Suppl. 97 (1935). Carridre. Die Schorgane der Thieve, vergl.- anat. dargestellte, Mlinchen (1885). Deyl. Bull, intern. Acad. Sci. Enip. Francois Joseph I, Prague (1895). Diicker. Jena. Z. f. Naturwiss., 60, 471 (1924). Franz. Zool. Jb., Alt. Zool. Physiol, 52, 118 (1932). Bolk's Hb. d. vergl. Anal. d. Wirbelticn, Berlin, 2 (ii), 997 (1934). Greeff. Graefe-Saeniiscli Hb. ges. Aiigen- heilk., Leipzig, II, 1 (2), Kap. 5, 74 (1900). Hageeloorn. ArcJi. AugenheilJ:., 102, 33, 393 (1930). Haller. Opera anatomici mi)ujra, 3 (1768). Hawes. Quart. J. micr. Sci., 86, 1 (1946). Hein. T. ned. Dierk. Vereen, 12, 238 (1913). Henckel. Bol. Soc. biol. Concepcion, Chile, 19, 69 (1944). Keibel. Z. mikr. Anat. Forsch., 12, 391 (1928). Kohl. Das Auge von Peiromyzon planeri iind von Myxine glutinosa, Leipzig (1892). Bibl. zool, 4 (13) (1892). Krause, R. Mikr. Anat. d. Wirbelliere. IV, Berlin (1923). Krause, W. Nacltriclilen Ges. Wiss. G. A. Unir. f.'ottingen. 23, 484 (1868). 644. 272 THE EYE IN EVOLUTION Krause, W. Arch. 7nikr. Anat., 12, 742 (1876). Kuhne. tlntersuch. a. d. physiol. Inst. d. Univ. Heidel, 1, 1, 15, 119, 341, 370 (1877-78). von Kupffer. Studien zur vergl. Entwick- lungsgeschichte d. Kopfesd. Kranioten : II Die Entwicklung d. Kopfes v. Am- vwcoetes planeH, Munich (1894). Langerhans. Vers, dtsch. Naturf. Aerzte, Wiesbaden, Sept. Atiat. Physiol., 69 (1873). Ber. Verh. naturj. Ges. Freiburg., 6(3), 1 (1876). Mann. The Development of the Human Eye, London, 274 (1928). Mawas and Magitot. Arch. Anat. micr., Paris, 14, 41 (1912). Miiller, H. Z. wiss. Zool., 8, 1 (1857). Wurzburg. naturwiss. Z., 3, 10 (1862). Miiller, W. Beit, zur Anat. und Physiol. (Festgabe C. Ludwig), Leipzig, 2 (1875). Plate. Allgemeitie Zool. u. Abstammungs- lehre, Jena, 2 (1924). Prince. J. comp. Neurol., 103, 541 (1955). Robertson. Biol. Rev., 32, 156 (1957). Rochon-Duvigneaiid. Les yeux et la vision des vertebres, Paris, 183 (1943). Schultze. Arch. mikr. Anat., 2, 175 (1866) ; 3, 215 (1867). Strieker's Hb. d. Lehre v. d. Geweben d. Menschen ii. d. Thieve, Kap. 26, Leipzig (1871). Steven. J. exp. Biol, 27, 350 (1950). Quart. J. micr. Sci., 92, 233 (1951). Stockard. A^ner. J. Anat., 6, 511 (1907). Studnicka. Anat. Anz., 41, 561 (1912). Tretjakoff. Bull, physico-math. Dept. Imp. Novoross. Univ., Odessa (1916). Treviranus. Vertnischte Schriften anat. u. physiol. Inhalts, Bremen, 3 (1820). Walls. Brit. J. Ophthal., 19, 129 (1935). The Vertebrate Eye, Michigan, 555 (1942). Walls and Judd. Brit. J. Ophthal., 17, 641 (1933). Young. J. exp. Biol., 12, 229 (1935). CHAPTER XI THE EYES OF FISHES No book on the comparative anatomy and physiology of the eye would be complete withovit a tribute to victor julius franz (1883-1950) (Fig. 286). The son of a famous astronomer in Konigsberg, he worked successively in Ziirich, Breslau, Halle, Frankfurt, Leipzig and Jena where he occupied the Chair of Phylogeny at the Ernst -Haeckel-Havis until after the World War when, in 1946, he was relieved of his post owing to his political associations with the Nazi party. From the time he gained his doctorate thesis on the anatomy, histology and function of the eyes of Selachians in 1905, his scientifle output was con- tinuous until 1944, and included such subjects as the anatomy of the eyes of Invertebrates and Vertebrates, particularly Acrania and Fishes, the anatomy and function of the brain of Fishes, the structure and function of jDigment cells, investigations into ocvilar functions such as phototaxis, accommodation and the light sense of a vast number of species, and a wide range of other kindred subjects. His systematic writings were also prolific, on comparative anatomy, evolutionary processes and, above all, on the structure and function of the organs of sight in the animal world. Compared with Cyclostomes, true fishes show many and con- siderable advances not only in their general structure as in the presence, among other things, of jaws, limbs (fins) and an exo-skeleton of scales from which teeth are derived, but also in their eyes which are more fully differentiated. The general co7ifignration of the eyes of Fishes exhibits structural characteristics which might at first sight appear to be peculiarities but most of them depend on the requirements of vision in water : it is to be remembered that the vertebrate eye initially evolved as an under- water visual organ (Figs. 287 to 291). In general, the globe is large, its size tending to vary with the depth at which the animal lives ; as a rule deep-sea fishes are provided with large eyes to receive as much light as possible in these dim regions — until, indeed, the absence of light in benthonic depths leads to the degeneration of the entire organ. ^ When a change of habitat occurs during development the size of the globe may vary accordingly ; thus the sunfish, Banzariia truncata. spends its larval life at great depths at which stage the eyes occupy one-quarter of the area of the body, but when the adults come to spend their lives near the surface their eyes become relatively quite small in maturity. A corresponding change occurs in the eye of the eel, Ang^iilla. which grows to a relatively enormous size before it migrates from its river habitat to breed and die in the Atlantic ocean. 1 p. 722. S.O.— VOL. I. 273 18 274 THE EYE IN EVOLUTION Fig. 286.— Victor Julius Franz (1883-1950). FISHES Figs. 287 to 291. — The Eyes of Typical Fishes. 275 Fig. 287. — The sturgeon, Acipenser sturio {Chondrostean). ..-^^r^ '% tA Fig. 288.- -The pike, Eso.r lucius (Teleostean). ^ >^!' J5>> Fig. 289. — The cod. Gndus morrhna (Teleostean). Fig. 290. — The ray. Raja clavata (Selachian). Fig. 291.— The dogfish, Squaluf aranthias (Selachian). (Reproductions of five of the beautiful engravings of D. W. Soenimerring, 1818. The reproductions are life-size and each represents the lower half of a horizontal section of the left eye.) Vision under water requires an eye relatively hypermetropic to vision in air ; moreover, the resistance of water while swimming is considerable and, therefore, as an optical and a streamlining device particularly among actively swimming fishes, the tendency is towards a flattening of the anterior segment of the globe. The typical section 276 THE EYE IN EVOLUTION of the fish-eye is therefore elhpsoidal with the shortest diameter the visual axis (Figs. 292 and 365) ; only in sluggish forms such as the bow-fin, Amia, does the globe become spherical. The maintenance of a non-spherical shape in the face of changes in pressure which may be considerable necessitates a sturdy outer coat ; the sclera therefore tends to be thick and is typically reinforced with a supporting layer of cartilage sometimes supplemented by bone. The flattening of the anterior segment implies a flat cornea ; but in a watery medium this structure is in any case useless as a refracting Fig. 292. — The Eye of the Trout. Note the flat shape with the short antero-iDosterior axis. agent. Perfection in its optical properties is thus neglected ; it is therefore often irregular and even ridged, and in the interests of strength is frequently thin centrally and thick in the jDeriphery giving it the construction of a sturdy arch. It follows that the entire responsibility for refraction falls upon the lens. The lens of fishes is consequently enormously large and almost spherical with a highly refractive nucleus and higher total refractive index (1-649 to 1-653) than in any other Vertebrate, making a maximal difference between it and the refractive indices of the other media. With the elimination of the cornea from the dioptric system and the dependence on the lens for refraction, it is necessary that a constant proportion should exist between the size of the leii ■ and its distance from the retina ; Matthiessen (1886), indeed, showed Miat this is so, that the eyes of fishes, no matter what their size ail liape, are standardized in their configuration, the distance from th'. ntre of the lens to the retina being constant (radius of lens FISHES 277 X 2-55 = Matthiessen's ratio). The lens has not only a light-refracting function, but in the absence of an optically effective cornea, it must also assume the onus of light -gathering. It is therefore typically situated far forward in the globe, bulging through the pupil and approximating the cornea. This large anteriorly-situated lens being an optical necessity, all other considerations of general configuration give place to it, and in cases wherein the globe would become too large to accommodate a lens of the required dimensions, as in some dec; _?a types frequenting an almost lightless habitat, the shape of the eye is changed from the ellipsoidal to a tubular form so that the large lens can remain at the required distance from the retina (Fig. 380). The large spherical lens makes accommodation by its deformation impossible, so that where an accommodative mechanism exists the expedient is adopted of moving the lens forwards or backwards — towards the cornea in the hypermetropic Selachians so that they accommodate for near vision, towards the retina in myopic Teleosts so that they accommodate for distance. The ciliary region is thus more specialized than in C!yclostomes giving rise to a suspensory apparatus for the lens and different tj'jjes of muscular structures to effect these changes in its position. The necessity of making as much use of the relatively small amount of light available in most watery habitats (apart from abyssal depths where no light is available) has led to the jacketing of the uvea of most pelagic and surface fishes with a mirror- like arrangement of guanine crystals to form the argentea, while the choroid of Selachians is provided with a tapetum lucidum ; an alternative seen in certain Teleosteans, is a similar deposition of guanine crystals in the jjigment epithe- lium (the retinal tapetum). While these form the main struc- tural characteristics of the eyes of Fishes, other advances are seen in com- parison with those of Cyclostomes, particularly the presence of an iris musculature so that the structure be- comes mobile, a considerably greater elaboration of the visual cells and the retinal structure, and myelination of the optic nerve fibres and the provision of septa within the optic nerve itself. Ant ON -apex SIR Fig. 293. — The General Scheme OF Fish Muscles (seen from the DoRS.\L Aspect). Ant, anterior part of orbit ; apex, apex of orbit ; LR, lateral rectus ; MR, medial rectus ; O, superior (and inferior) oblique ; ON, optic nervp ; SIR, superior (and inferior) rectus. 278 THE EYE IN EVOLUTION As in all Vertebrates below Mammals the decussation of the optic nerve fibres at the chiasma is total. ^ An area centralis, exceptional in Selachians, is commonly seen in Teleosteans and in a number of particularly agile littoral types of this class a fovea is present. The ocular movements in Fishes are in general restricted, reflex and primitive, and the extra-ocular muscles are essentially designed to subserve rotations of the eyes compensatory to movements of the body ; with few exceptions ^ fixation is attained, not by movements of the eyes but of the body in swimming. The muscles are therefore designed to subserve merely the simple rotations required by the postural mechanism ; the recti form a cone arising from the apex of the orbit, and the obliques, subserving simple wheel-rotations, arise anteriorly and remain on a plane anterior to the recti (Fig. 293). The super-class of Fishes includes an enormous number of forms, many of them long since extinct ; the extant types may be divided into two main classes^ : (a) CHONDRiCHTHYES ()(6v8pos. Cartilage ; l^dvs, a fish) (or elasmobranchs — eAaa/i,o9, a metal plate ; branchia, a gill ; so called because of their lamelliform gills) with a cartilaginous skeleton, and {b) OSTEICHTHYES (dcTTeov, bone ; l^Ovs, a fish) with a more or less ossified skeleton. CHONDRICHTHYES (or cartilaginous fishes) are represented today only by two sub-classes — the selachii (CTeAa;;^os', a cartilaginous fish) which include the families of sharks and skates or rays, and the holocephali (oAo?, whole ; K€ -The pupil of the dogfish, Scylliorhinus. traction (after Franz). Showing stages of con- Heterodontus arrangement of the musculature of the iris ; when this forms a con- tinuous sheet a round or oval pupil results ; where this is lacking in certain areas an operculum is formed (Grynfeltt and Demelle, 1908). Of the first type, some deep-sea species (the luminous shark, Etmopterus; C'enirojjhorus calceus) have large, round, almost immobile pupils with poorly developed muscles — a configuration to be expected in their dimly lit habitat. Species which come to the surface and bask have contrac- tile pupils, usually circular in dilatation and elliptical on contraction (characteristically in the vertical direction but sometimes oblique or FISHES 287 horizontal)^ (Figs. 303 to 312). Amongst fishes this shape of pupil is characteristic only of Selachians. An expansible opeeculum, a structure described by Cuvier (1805) and subsequently by Leuckart (1875), is a feature of the flattened Batoidei with their upward-looking eyes ^ ; it is a structure on the upper part of the pupillary margin which expands downwards in bright light to block the aperture so that the eyes appear to " close." The mechanism whereby this non-muscular structure contracts and exjDands is unknow^l. These opercula are of varying shapes : thus the contracted pupil of the electric ray, Torpedo, or the spotted dogfish, ScyJliorhinus, is a horizontal slit divided in the middle by a tiny operculum (Fig. 313) ; the operculum may be provided with a smooth edge, as in the sting-ray, Trygon, and Torpedo, or the margin may be serrated as in other members of the ray family {Raja clavata, R. bat is, Trygono- rkina and others), so that on full expansion it reduces the pupil to a crescent of stenopoeic apertures (Fig. 312). The voluminous leyis is never completely spherical as in Teleosteans, but is always lenti- cular in shape with the transverse diameter slightly greater than the antero-posterior. Un- like the cyclostome lens and as occurs in all other Vertebrates except lizards, a system of sutures is present ; it is, however, very simple consisting merely of a single line- suture rumiing vertically in the anterior part and horizontally in the posterior 3 (Rabl, 1898) (Fig. 314). The epithelium clothing the anterior surface is continued beliind the equator, whereafter, as m other ^>rtebrates, the cells are prolonged into fibres, the nuclei of which lie in the posterior cortex. The vitreous is of a dense consistency particularly in its anterior parts where it forms the susjDensory apparatus of the lens ; it has little adherence to the retina posteriorly whence it is readily detached. The retina has received a considerable amount of study. "^ In the embryo, blood vessels lie in the foetal fissure (de Waele, 1900) but these disappear and in the adult the retina is quite avascular and shows no trace of the foetal fissure except a tiny wliite area on the summit of the ciliary papilla (Fig. 301). The retinal epithelium is comprised, as is 1 The basking shark, Selache ; the spiny dogfish, Squalus ; the porbeagle shark, Latnna ; and so on. 2 Thus it is absent in the devil-fisli rays, Mobuhda?, wliich have lateral eyes and also in the dorso-lateral eyes of Myliobatis. 3 A single line-suture is found also in the lenses of most Teleosts, Anurans, Reptiles, some Birds and the rabbit. * Krause, 1886-89; Xeumayer. 1897; Schaper, 1899; Greeff, 1899; Addario, 1903 ; Retzius, 1905 ; Schnaudigel, 1905 ; Franz, 1905 ; Verrier, 1930 ; and others. Fig. 314. — Lenticular Sutures of Selachians. Showing the vertical anterior suture. Pos- teriorly there is a short horizontal suture. Sci/lliorhinus Raj.t 288 THE EYE IN EVOLUTION usual, of a single layer of hexagonal cells, but when a tapetum is i^resent these are unjiigmented until the ora is reached in order to allow the passage of light to tliis structure (Fig. 315). The architecture of the retina itself is simple with the usual layering, but a considerable scattering of cells outside the confines of their layers may occur. The horizontal cells are unusually massive (like those of the lamprey) and ganglion cells are sparse. Characteristically the retina, is pure -rod, the Fig. 315. — The Selachian Retina. The retina of the ray, Raja maculata. 1, pigment of choroid ; 2, (non-pigniented) retinal epitheUum ; 3, laj'er of rods ; 4, external limiting meinbrane ; 5, outer nuclear layer ; 6, inner nuclear layer ; 7, nerve fibre layer (Mallory's trijjle stain) (Katharine Tansley). Fig. 316. — The Cone and Rod OF THE Dogfish, JVffsri.;7.f.s'(xlOOO) (Gordon Walls). Squatina cells being thin and long ; the ratio of visual to ganglion cells varies (152 : 1 in Efmoptenis, 14 : 1 in Myliohatis, 12 : 1 in Raja miraletus — Verrier, 1930). There is no area centralis, although in some species, jiarticularly the dogfish, Mustelus, the density of the visual elements is increased in a round central area so as to suggest an elementary precursor of this characteristic of the higher Vertebrates (Franz, 1905) (Fig. 317). Only in a few particularly active species are cones found — the dogfish, Mustelus, the eagle-ray, Myliohatis, and the angel-shark, Squatina (Franz, 1905 ; Verrier, 1930 ; Rochon-Duvigneaud, 1943) (Fig. 316). The optic nerve has various septal patterns and in some species an cpendymal core, as in lampreys (Prince, 1955) ; like the retina it is avas lar. The optic disc is small and flat and a lamina cribrosa is FISHES lacking. Unlike those of the lamprey, the optic nerve fibres have become myelinated (Bruesch and Arey, 1942). At the chiasma there is a complete crossing of the nerve fibres, frequently in the form of interlacing bundles (Figs. 318 and 319) (Verrier, 1930). THE EXTEA-ocTJLAR STRUCTURES. The jDresencc of mobile eyelids, both upper and lower, sometimes with an additional fold constituting 289 Fig. 317. — The Area Centralis {ac) of the Dogfish, Mustelvs. Xote the increase in length and concentration of the visual cells and the great number of ganglion cells (after Franz). a third or nictitating membrane in many selachian species is a curious anomaly in the eyes of a fish (Fig. 299). These structures are supplied with an elaborate musculature blended with the muscles of the spiracle; a superficial layer comprises a retractor palpebrse superioris and a con- strictor spiraculi, and a deep layer consists of a levator palpebrse nictitantis, a depressor palpebrae superioris and a dilator spiraculi, the Figs. 318 and 319. — The Chiasma of Selachians (Verrier, 1930). Fig. 318. — The dogfish, Squalus. Fig. 319.— The skate, Raja. different elements being more or less blended. The palpebral muscles are supplied by the seventh nerve, the muscles of the nictitating mem- brane by the maxillo-mandibular division of the trigeminal (Ridewood, 1898 ; Harman, 1899-1903). The lids are well developed in the deep- sea sharks of the requin family {Galeorhinus) wherein the outside of the nictitating membrane is clothed with the same type of minute placoid scales as is the outer surface of the lower lid. Occasionally there is merely an immobile circular lid-fold in which case a nictitating membrane alone is present (the bonnet shark, Sphyrna tihuro). The purpose of these elaborate lids is difficult to imagine ; Franz (1905) concluded that they were not used to escape from the dazzling of bright light. 290 THE EYE IN EVOLUTION The orbit is cartilaginous and usually very incomplete ; in it the eye lies in a bed of gelatinous connective tissue rich in blood sinuses. The extra-ocular muscles are simple — four recti form a cone inserted into the globe about its equator wliile the two obliques, arising close together, sweep round the anterior part of the globe in front of the recti and are inserted in common with the vertical recti. These muscles may be enormously developed in the larger sharks ; in the basking- shark, Selache, for example, they are as thick as the biceps of the average man. The most characteristic structure in the orbit, however, is the peculiar optic pedicle, a prop-like cartilaginous structure which runs from the cranium to the posterior pole of the eye which it receives in an expanded cupped head, thus forming a simple ball-and-socket joint (Figs. 290 and 298). The globe in its cartilaginous sclera thus receives a firm support. Sometimes the pedicle is firm and stiff ; in some sharks and rays it is slender, bending when the extra- ocular muscles contract, straightening and proptosing the eye when these relax. Sometimes it is incomplete, either not reach- ing the eye or the cranium (in the elongated orbit of the hammerhead shark, Sphyrna zyqcena) (Fig. 387), Fig. 320.— The head of the rabbit-fish, • i , i i i • /xi, Chimcera monstrosa (Bland-Sutton's O^ mdeed, may be lacking (the Lectures and Essays, Heinemann). spotted dogfish, ScylUorMnus) . THE HOLOCEPHALIAN EYE THE HOLOCEPHALiANS are represented today only by the Chimseras (rabbit-fishes or ghost-sharks), somewhat shark-like fish of wide distri- bution and very primitive in type (Fig. 320) ; they are all deep-sea bottom fishes, and their eyes, which are of the same type as the selachian eye, are remarkable for their adaptation to the dim illumina- tion of the ocean depth. For this reason the pupils are large, round and almost immobile, a tapetum is lacking, and the retina has an unusually dense population of rods summated by an unusually small number of ganglion cells (100,000 rods per sq. mm. and 600 ganglion cells, Franz, 1905) — a ratio not exceeded amongst Selachians except in the abyssal forms such as the luminous shark, Etmopterus. The shape (f the eye is the typical ellipsoid of the selachian eye but, curious • the sclera is thin, sometimes apparently discontinuous. FISHES 291 Osteichthyes THE TELEOSTEAN EYE TELEOSTEAXS are a huge and diversified class which comprises the great majority of modern fishes. Ocularly — and in many other respects — they show the highest differentiation among fishes, exhibiting many anatomical and physiological characteristics which are peculiar to themselves. Figs. ,321 and 322. — Typical Teleostean Fishes. Fig. 321. — The cai'p, Cyprinus (photograph by Michael Soley). Fig. 322. — The mouth-ljreeder cielihd, CicJiIa (Zool. Soo., London). Although there are great variations among the many sjDecies. tlie teleostean eye has certain essential characteristics (Figs. 323-4) : an mcoiuplefe civp of hijaUne scleral cartilage, and a tendevcy to multi-layering of the cornea ; a very elaborately developed annidar ligament bridging the angle of 292 THE EYE IN EVOLUTION Caraasius the anterior chamber between the cornea and the iris, and a tensor choroidece muscle ; the presence of a choroidal gland in most species ; a failure in closure of the foetal fissure allowing the protrusion of the choroid through the retina as the falciform process [or alternatively the emergence of a hyaloid system of vessels) to nourish the inner layers of the retina, which with one known exception {the eel) is avascular ; an ectoderynal retractor lentis muscle at the distal end of the falciform process ; the frequent presence of a choroidal tapetum (argentea) usually of the lucidum type, but sometimes cellular, neither type, however, having a visual function since they are masked by the pigment epithelium of the retina ; a pupil usually immobile and often so large as to leave an aphakic aperture ; a highly organized retina typically containing both rods and cones as well as double cones, and sometimes a fovea. THE GENERAL SHAPE OF THE TELEOSTEAN EYE USUally COnformS to the standard type characteristic of Fishes ; in most species it is an anteriorly flattened elHpsoid with the antero -posterior diameter shorter than the transverse, although in slow-swimming and small-eyed types the shape tends to be more nearly spherical. An exception to this occurs in certain deep-sea Teleosts. In these dark regions the poverty of the illumination requires an immensely large lens, to accommodate which the globe may acquire a tubular shape. ^ Other benthonic Teleosts, giving up the struggle to make use of light in their dark environment, have vestigial eyes, often covered with opaque skin ^ — one deep-sea Teleost (the only known Vertebrate in such a case)has no eyes {Ipnops); as an accessory, certain benthonic fishes have developed luminous organs, sometimes in association with their eyes, with which they make contact with their kind.^ The sclera is a fibrous tunic sometimes tenuous and thin (as in the goldfish, Carassius auratus), sometimes immensely thick (tjie star-gazer, 1^ Astroscopus), reinforced by hyaline cartilage which sometimes becomes partly ossified (Yatabe, 1932 ; Rochon-Duvigneaud, L943 ; Woelfflin, 1955) : only in a few forms is cartilage lacking (some eels, Gymnotidae ; the pearl-fish, Encheliophis) . Instead of forming a complete cup as in Selachians, however, the cartilage is lacking in the posterior part ; the general arrangement is therefore the opposite to that which occurs in Birds in which the posterior segment of the sclera is reinforced by cartilage (Fig. 327).* Its extent varies considerably ; sometimes it is confined to a relatively narrow ring around the limbus (the salmon- trout family, Salmonidae) or the equator ; sometimes it clothes the 1 p. 332. ■ p. 722. 3 p. 736. ^ p. 403, Fig. 496. FISHES Figs. 323 and 324. — The Teleostean Eye. 293 Fig. 323. — Diagram of a Teleostean eye. AC, autochthonous layer of cornea ; AL, annular ligament ; CE, corneal epithelium ; CG, choroidal gland ; CH, campanula of Haller ; FP, falciform process ; LB, lentiform body ; OX, optic nerve ; S, scleral cartilage ; Sc, sclera ; SC, scleral cornea ; SL, suspensory' ligament ; TC, tensor choroidese. \ ■(, Fig. 324.- -The eye of the trout. In the section the dermal layer of the cornea has come loose, as usuallj^ occurs (Norman Ashton). 294 Mormyrid THE EYE IN EVOLUTION entire eye apart from a small fibrous zone around the oiDtic nerve (the soles, Soleidpe) ; sometimes it forms discontinuons islands (the elephant- fish family, Mormyridse) ; sometimes it becomes partially calcified, and exceptionally, as in Tetragonopterus, this transformation is com- plete. Scleral ossicles formed of true bone are also usually found, typically as thin plates embedded in the fibrous tissue of the sclera, situated temporally and nasally anterior and external to the cartilage ; occasionally in active types with large eyes these combine to form a complete osseous ring of considerable strength (the sword-fish, Xiphias ; tunny, Thuimiis).^ Fig. 325 — The Cornea of the Carp. iShowing the thick epitheHuni (Smelser and Chen). Xiphias Minnow The cornea, usually elliptical with the long axis horizontal, (Grynfeltt, 191 () : Verrier, 1927). is frequently irregular and grooved and has a variable constitution. In some forms it shows the usual vertebrate configuration, the substantia propria being relatively homogeneous (Salmonidce — salmon, trout ; Cyprinidse — minnows and carps ; Esocidae — pike) (Fig. 325) ; but in others it is uniquely complex, 4 layers being readily distinguishable : (1) A dermal layer, derived from and continuous with the skin, consisting of a multi-layered, usually thick ejiithelium. Bowman's membrane and the superficial portion of the substantia propria. ^ It is to be remembered that the scleral ossicles of Sauropsida are homologous not with the scleral ossicles of fishes, but with the circumorbital bones. The ossicles of tli(> sturgeon are derived not from the sclera but from the skin (H. Miiller, 1872), p. 317. FISHES 295 (2) An intermediate layer between the dermal and scleral portions corresponding topographically to the episcleral tissue. It consists of very loose lamellar tissue, so loose that it readily allows the superficial layer to be peeled from the deeper and occasionally permits some degree of movement of the globe under the dermal cornea (the eel, AnguiUa) (Hein, 1913). It is interesting that on luxation of the eye the scleral cornea readily splits from the dermal so that the latter may remain in place and be left behind (Rochon-Duvigneaud. 1916) (cf. Fig. 324). (3) A scleral layer consisting of dense lamella' of substantia propria structurally continuous with the sclera itself. (4) Descemet's membrane and its endothelium of extreme delicacy. In some species, indeed, the endothelium and Descemet's membrane appear to be absent in the central area of the cornea (carp, Cyprinus — Smelser and Chen, 1954) (Fig. 325). So far this arrangement somewhat resembles that seen in lamprej's,^ and appears to be more primitive than the typically vertebrate selachian cornea. In some species, however, there is an apparently separate layer of coarse fibres on the inner aspect of the finely lamellar scleral layer — the autochthonous LAYEK of Leuckart (1876). It thickens greatly towards the periphery and termin- ates abruptly at the scleral margin, but is probably merely a modified portion of the scleral cornea. An interesting phenomenon is the occurrence of yellow pigmentation in the corneae of many Fishes due to the presence of xanthophores in the ei^ithelium. In the bull-head. Coitus, for example, there is a pigmented process running over the cornea like a yellow waterfall (Walls and Judd, 1933), while the entire cornea of the carp, Cyprinus, and the jDike, Esox (Schiefferdecker, 1887) is yellow. It is interesting that Soemmerring (1818) in describing this appearance originally, attributed it to a yellow aqueous humour. The pigment must act as a light - filter as does yellow pigmentation in the lens.- A regular feature of the teleost cornea is an accumulation of cells, apparently continuous with the endothelium, which fills the angle of the anterior chamber and is reflected over the surface of the iris to form a massive axnular ligament (Angelucci, 1881 ; Lauber, 1901), the " vesiculo -hyaline tissue of the angle " of Rochon-Duvigneaud (1943) (Fig. 326) ; from it the tensor choroidete muscle is probably derived. The annular ligament, somewhat reminiscent of the endothelial proliferation seen in Cyclostomes and Chondrosteans, is elaborately developed in Teleosteans. It is composed of large polyhedral epithelioid cells (Giacomelli. 1935) ; it may be vascularized (the mud-skipper, Periojihthalmus^) or contain melanophores (the cod, Gadus) and is sometimes rich in lymphatic sinuses which, however, cannot be considered homologous with the canal of Schlemm (Franz, 1910 ; 1 p. 265. ^ Compare the yellow pigmentation in the cornea of the bow-fin, Ajyiia, in the lenses of the lamprev and of diurnal snakes and squirrels, or yellow oil-globules in some retinal cones (p. 656). » p. 326, Fig. 386. 296 THE EYE IN EVOLUTION Karsten, 1923). Not only does this layer cover most of the anterior surface of the iris, but in a few Teleosteans it appears to form a thick stratum, in part fibrillar, in part cellular, on the inner aspect of the scleral cornea — the supplementary layer of Rochon-Duvigneaud Fig. 326. — The Angle of the Anterior Chamber of the Trout. Showing the immense thickening in the periphery of the cornea and the annular ligament filling up the angle of the anterior chamber and binding the iris to the cornea. The dermal layer of the cornea (as often occurs) has been lost ( X 84) (Norman Ashton). 11 (1943) (goby-fishes, Gobius niger, Periojjhthalmus ; the soles, Soleidse, etc.). Various views have been put forward as to the nature of this structure which may add another layer to the already complex cornea Qobius and appears topographically to be continuous with the choroid ; a secretory function has been suggested, but r its exact significance must await further study (see Ballowitz, 1913 ; Kolmer, 1913 ; Remotti, 1929 ; Schaffer, 1929 ; Baecker, 1931). The uveal tract shows several distinctive characteristics (Fig. 327). The choroid has the essential vertebrate structure of a chorio- capillaris and a heavily pigmented vascular layer, but is noteworthy for three features — the argentea, the choroidal gland and the falciform process. In the majority of pelagic forms there is a layer of guanine-laden cells interspersed with chromatophores — the argentea — jacketing the outside of the choroid with a silvery coat which is continued forwards over the anterior surface of the iris giving it its metallic appearance. In view of the fact that it is obscured from the retina by pigment, this layer can have no visual value ; Fig. 327. — Section through THE Equatorial Segment OF THE Eye of the Trout. Showing the thick choroid, ch, the retina, r, and the scleral cartilage, s (Feulgen ; X 6; 'Katharine Tansley). FISHES 297 Figs. 3:28 and 329. — Thk Chokoidal Gland of the Trout, Salmo trutta (Xorman Ashton). Fig. 328. — The " gland " occupies the upper part of the figure ( X SO). Fig. 329.— Structure of the -'gland" ( X 320). it is possible that it serves a protective disguise in tloe transparent larva the black eyeball of which would otherwise be dangerously conspicuous, blending with the reflexes of the water m the same way as do the silver reflections from the sides of the adult fish. In a few^ species there is, in addition, a tapetum fibrosum on the inner aspect of the choroid separating the main vascular layer from the choriocapillaris, such as is typical of hoofed Mammals (Millot, 1923) ^ : it is composed of a layer of dense fibrous tissue of a glistening tendon-like structure wherein the ' p. 457. 298 THE EYE IN EVOLUTION Figs. 330 and 331. — The Falcifobm Process, in an Adult Teleostean (Trout). ""^ W ' ^^ • / ^\yV ^ \-^^ r^^y ^""""•'Sii^^-L^^K^^^ u ^<^^::ip>^ Fig. 330. — The macroscoiDic intra-ocular ajDpearance of the posterior half of the globe seen from the front. F, falciform process. Fig. 331. — Section across the region of the fcetal fissure. H, vascular mesoderm of the falciform process ; E. neuro-ectoderm of the wall of the oj^tic cup (Mann, after von Szily). other choroidal constituents (pigment cells and vessels) have been cut down to a minimum (Walls, 1942). The CHOROIDAL C4LAND, an organ so called by Cuvier (1805) but with no structural or functional affinities to a gland, is a peculiar vascular formation lying in the posterior part of the globe between the choioid and the sclera (Figs. 328-9). It is highly vascularized, consistiim essentially of a mass of juxta-apposed capillaries sometimes forming a ring around the optic nerve, more frequently horse-shoe-shaped in whicii se the open end of the horse-shoe, ventral to the nerve, may FISHES 299 be partially filled by a similar accessory body, the lentiform body. It occurs in the majority of Teleosteans (Erdl, 1839) — according to J. Miiller (1840), in all those provided with the hyoid gill (or pseudo- branch) from which it is directly supj^lied with highly oxygenated arterial blood ; from the "gland" the blood flows into the choroidal circulation. Both the pseudobranch and the choroidal gland are absent in some genera with small eyes, such as the eels [AngnUla) and the cat -fishes (Siluroids). It has been suggested that the choroidal gland forms a special mechanism whereby the circulation is maintained despite considerable changes in pressure when rapid alterations occur in the dejith of swimming (Allen, 1949) ; this, however, seems unlikely in view of its constant presence whatever the habitat of the fish. Nor does it appear to act as an erectile organ assisting accommodation by pushing the retina forwards (Barnett, 1951 ; Yamasaki, 1954) ; it is probably pvirely nutritive in function. Anguilla Cat-fish The vascularisation of the inner eye is further maintained by the falciform process, or when it is absent, by a hyaloid system of vessels. The FALCIFORM PROCESS is a peculiarity of Teleosteans and consists of a prominent sickle-shaped ridge of pigmented and richly vascularized choroidal tissue which j^rotrudes through the inferior part of the retina in the region of the foetal fissure (which has never closed), running from the optic disc to the ciliary region (Figs. 330-1) (Franz, 1910). This structure is somewhat analogous to the cone of Reptiles and the pecten of Birds although these structures are ectodermal in origin and are secondarily vascularized. In some species the fissure has closed posteriorly so that only the anterior portion of the falciform process remains (the cod. Gadns : herring. Clujiea : carp. Cyprinus : etc.). In those species in which the process is small or absent, as in certain eels (conger. H. Virchow, 1882), cyprinoids such as the carp and roach (O.Schultze. 1892), and goby fishes (Karsten. 1923), the nutriment of the inner eye is taken over by a hyaloid system of vessels which, like the falciform process, issues through the foetal fissure : the main artery enters the eye in the region of the oj^tic disc and instead of running through the choroid to constitute the basis of the falciform process, breaks into the superficial layers of the vitreous and forms a dense vascular plexus running anteriorly lying loosely upon the inner surface of the retina (Chrustschoff, 1926) (Figs. 332-3). This membrana VASCULOSA retix.e Constitutes an arrangement of widespread dis- tribution among Vertebrates and is comparable to that seen in certain Amphibians and Reptiles (snakesj. It is to be noted that these vessels ramify in the vitreous, lying superficially on the retina without entering it. The veins drain anteriorly into an annular vein which leaves the eye through the ciliary zone, and between tlie two a widely- Gadus Clupea harenytxs 300 THE EYE IN EVOLUTION meshed net is spread in which the capillaries are associated with the AT^eins leaving a zone free of small vessels around the arteries. An exception of more than usual interest is seen in the ee\,Anguilla. This fish is unique in having no demonstrable choroid, for the large cells of the retinal pigment epithelium lie directly on the sclera, and as if in compensation the vessels of the membrana vasculosa vascularize the retina directly (Fig. 334) (W. Krause, 1876 ; Virchow, 1882 ; Denissenko, 1882 ; Michaelson, 1954). The vessels of this membrane Figs. 332 and 333. — The Membrana Vasculosa Retinae of Teleosteans. Fig. 332. — In the goby fish, Gobius poecilichthys. The vessels emanate from the central artery of the retina and run over this tissue within the vitreous. The division of the prin- cipal vessel into the annular vein is seen on the nasal side, at V (after Karsten). Fig. 333. — Sketch of injected retina of the roach, Eutihis, .showing the concentra- tion of capillaries around the vein (to the left) while the peri-arterial zone (to the right) is relatively free from capillaries ( X 23) (I. C. Michaelson). derive from a large central artery entering the eye, as is usual, through the optic disc and its branches form an arterial network in the vitreous lying on the surface of the retina and extending to the periphery of the fundus where they form capillary loops. From this arterial network numerous branches pass from the vitreous through the internal limiting membrane into the retina : Virchow (1882) estimated that there were 9,600 of them. In the substance of the retina they divide into two strata of capillaries, one in the inner and one in the outer nuclear layer, and from these retinal capillary nets blood is drained by large veins which combine to form four main vessels and eventually join to fdrni a central vein in the optic nerve head (Figs. 334 and 335). The abs; iice of a choroid in this fish is unique and the direct vasculariza- tion oft inner retinal layers constitutes the only known exception FISHES 301 Fig. 334. — Section of the Eye of the Eel. The superficial vitreous and both retinal capillary nets can be seen filled with indian ink (»■). The cells of the retinal epithelium form a broad layer. There is no choroid present, the epithelial layer lying directly on the cartilaginous sclera (s) ( X 169) (I. C. Michaelson). Fig. 33o. — The Retina of the Eel. Injected with indian ink, mounted in glycerme. The superficial vitreous vessels are in focus : these are arterial ( y. 37) (I. C. IMichaelson). to the general avascularity of the teleostean retina ; indeed, it is the only known case in which the vertebrate retina is directly vascularized except in the colnbrid snake Tarbophis and in Mammals. The ciliary zone is narrow and, without folds or processes, may be said not to exist so that the choroid apjoears to i3ass directly into the iris (Fig. 336)1; only in a few amphibious types such as Anahhps do a few processes exist. This region, however, provides the supporting and accommodative apparatus of the lens. Dorso-nasally the latter ^ See footnote p. 267. 302 THE EYE IN EVOLUTION is suspended pendulum-like by a firm suspensory ligament, a con- densation of the anterior vitreous with a fibrillar appearance on microscoj)ic examination (Harms, 1928 ; Teulieres and Beauvieux, 1931 ; Koch, 1952). Ventrally, at the ciliary end of the falciform process, a small structure of great variability in size and shape makes contact with the lens by ligamentous condensations of the vitreous — the CAMPANULA of Hallcr (1762). It contains a triangular muscle of smooth fibres of ectodermal origin being derived from the retinal epithelium of the ciliary zone at the open lips of the fcetal fissure, thus resembling in this respect the muscles of the iris (Nussbaum, 1901 ; V. Szily, 1922), and is innervated by a short ciliary nerve from the Fig. 336. — The Anterior Segment of the Eye of the Bull-head, CoTTVS BCBALIS. i, iris ; si, suspensory ligament ; s, serous spaces behind the annular liga- ment ; ca, scleral cartilage ; co, conjunctiva ; c, cornea ; p, posterior layer of the cornea ; CH, campanula of Haller (after a drawing by Rochon- Duvigneaud). Scorpcena ciliary ganglion (TretjakofF, 1926 ; Meader, 1936). It has been generally accepted as being the effector muscle in the accommodative mechanism, acting by retracting the lens towards the retina, a claim, however, contested by Bourguignon and Verrier (1930) who failed to find muscular tissue in this somewhat peculiar structure. Whatever its true nature, it is a characteristic of Teleosteans, being absent only in a few species such as the eel. An additional muscle is found in this region in practically all species — the tensor CHOROiDEiE. It was initially described as being composed of fibrous tissue and named the " ciliary ligament " (Leydig, 1853 ; Leuckart, 1876), but has been shown to contain smooth muscle fibres (Grynfeltt, 1910 ; Rochon-Duvigneaud, 1943). It is a tenuous muscle, about 1-5 mm. in length, lying between the sclera and the uvea, arising from the annular ligament anteriorly, thus clioring itself to the cornea, and inserting itself into the anterior i^ ri of the choroid just behmd the ora (Faravelh, 1890-91 ; Grynfeltt, It;'') ; in the scorpion-fish, ScoriKena, there is an additional shp PLATE II Thk TiuDES OF Teleosts (Ida Mann) I Fig. 1. — The kilJifish, AiAodieiliditliys ruiirostKjmfi. Fig. 2. — The salmon. S