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TEXT-BOOK OF EMBEYOLOGY

MACMILLAN AND CO., LIMITED

LONDON • BOMBAY • CALCUTTA
MKLBOURNE

THE MACMILLAN COMPANY

NEW YORK • BOSTON • CHICAGO
DALLAS • SAN FRANCISCO

THE MACMILLAN CO. OF CANADA, LTD.

TORONTO

i-

TEXT-BOOK

OF

EMBRYOLOGY

VOL. I

INVERTEBRATA

BY

E. W. MAcBEIDE, M.A., D.Sc., LL.D, F.R.S.

PROFESSOR OF ZOOLOGY AT THE IMPERIAL OU.r.EcjR OF SCIENCE AND TECHNOLOGY

SOUTH KENSINGTON

EDITED I'-V

WALTER HE APE, M.A., F.K.S.

MARJN£
BiOLOGJCAL
LABORATORY

LIBRARY

WOODS HOLE, MASS.
W. H. 0. i.

M ACM ILL AN AND CO, LIMITED
ST. MARTIN'S STREET, LONDON

1914

COPYRIGHT

TO
THE MEMORY OF

ADAM SEDGWICK

BELOVED TEACHER AND FAITHFUL FRIEND

THIS VOLUME

IS DEDICATED BY THE

AUTHOR

Uj[UiRARYl2]

<?&

PREFATORY NOTE

THE design of this Text-book of Embryology, of which this is the
first volume, is to associate the structural development of embryos
with broad generalizations of what is known of their physiology.
Attention will be drawn, for instance, to the correlation between
the function of certain organs of a larva and its habit of life, and,
in a more general way, between function and habit and the course
of development. Reference will be made to some of the more
striking results obtained by Experimental Embryological research.
Attention will be drawn to gaps in our knowledge which indicate
promising fields for research.

It is hoped that the interest of all students of Embryology will
thus be stimulated, and the practical value of these volumes,
especially for students of medicine, ensured.

A second volume, by Professor Graham Kerr, in which the lower
Vertebrata will be dealt with, will follow as soon as possible, and
a third volume by Mr. Richard Assheton, on Mammals, will complete
the work.

The Authors are responsible for the facts and generalizations
recorded, and to them is due all the credit which may be given
to the work.

THE EDITOR.

vn

7LU LIBRARY -*

:\ <*+*» J*y

I

* ,' t ^^*--- ,?

«..

PREFACE

THIS book has been written in order to achieve two objects, first to
place before the reader in as succinct a form as possible the best ascer-
tained results in the field of Invertebrate Embryology, and secondly
to indicate some of the problems which as yet remain unsolved and
the best, means of attacking them.

In order to attain the first object a number of typical life -histories,
illustrating all the important groups of Invertebrata, have been
described, and in selecting the types for special description two
principles have guided us : first, the life-history of the type chosen
must be thoroughly ascertained, and second, the type must be a
common form easily accessible to students in temperate regions.
Thus the spider has been chosen as a type of the Arachnida rather
than the scorpion, and for the same reasons the life-histories of
parasitic forms have been very slightly dealt with. The Trematoda
and Cestoda have been entirely left out of consideration because it
is difficult to obtain a complete series of the stages in the life-history
of any one species — and though the external features of the life-
history of members of these groups are known, their organogeny is
still to be worked out. Moreover, the external features of the
development of Trematoda and Cestoda are adequately described in
ordinary text-books of zoology.

In pursuit of the second object the methods used by the best
investigators have been given in connection with the description of
the life-history of each type examined by them, and we have ever
striven to keep before the mind of the student the idea that the
ultimate object of the Science of Embryology is not solely the
ascertaining of facts but especially the determination of the laws of

IX

x INVEKTEBKATA

life which underlie them ; it is for these reasons we have endeavoured
to make full use of the light which the new science of Experimental
Embryology throws on these lawTs.

In a book of this compass, devoted to such an enormous subject
as Invertebrate Embryology, very much must necessarily be omitted,
but it seemed to us better to run the risk of criticism on this score
and to bring our survey of the field to a conclusion within a reason-
able period, rather than to attempt to give a complete account of all
that is known of Invertebrate Embryology. Such an attempt would
involve the task of writing not a single volume but a series of
volumes ; it would require for its accomplishment many years and
would be beyond the powers of one man. Moreover, the first volume
would be out of date long before the last volume was published.

The literature lists have been purposely kept as brief as possible

—as a rule only the most recent papers on the subject have been cited.

Where earlier papers have been referred to it is chiefly because these

papers, in laying the foundation of our knowledge, have not been

superseded by later work.

In conclusion, my best thanks are due to my colleagues, Professor
Lefroy and Mr. Dobell, for valuable suggestions, and to my wife for
much help in the tedious work of preparing the Index.

E. W. M.

IMPERIAL COLLEGE OF SCIENCE, SOUTH KENSINOTOX,

, 1914.

CONTENTS

CHAPTER I

INTRODUCTION

Scope of Embryology — Growth, maturation, and conjugation of the germ-cells — Sex-
chromosomes and their bearing on theories of heredity — Recapitulation theory
of development and the evidence in its favour — Embryonic and larval phases of
development and their mutual relationship — Factors modifying the course of
development ..... . . Page ]

CHAPTER II
PRACTICAL HINTS

Methods of preserving embryos — Methods of embedding embryo for section-
cutting and of orientating them so that the sections shall be cut in a known
direction ...... Page 32

CHAPTER III

PORIFERA

The development of Sycnndrn raphanus as a type of the Calcarea : the Blastula,
Amphiblastula, and Ascon stages in its development — The development of other
sponges (Oscarella, Plakina, Espcria, Sponyilla, Clathrina, Leucosolcnia] —
The development of the gemmule of Epli-iidatia — The ancestral history of
sponges ...... . . Page 37

CHAPTER IV

COELENTERATA

The development of T/ibularia as a type of the Hydrozoa — The development of the
eggs of free-swimming medusae — The development of the gonophore of Tubnluriii
and of the medusa of Podocoryne — Other gonophores — The development of
Siphonophora, Narcomedusae, and Trachymedusae — The development of Aur<l'm
as a type of the Scyphozoa — The development of Pelarjia — The development of
Urticina as a type of the Actinozoa — The development of Aflinln berimidensis —
The larvae of Zoanthidae and Cereanthidae — The development of Alcyonaria — The
development of the skeleton of Caryophyllia — The development <>l l'» roe ;is ;i type

xi

xii INVERTEBRATA

of llie Ctenophora — The formation of the tentacles of C'allianira — The affinities
of the Ctenophora with other Coelenterata — The experimental embryology of
Coelenterata — The ancestral meaning of the Planula larva . Page 53

CHAPTER V

PLATYHELMINTHES

The Polyclada the most primitive group of Platyhelminthes so far as their develop-
ment is concerned — Development of Planocera inquilina as a type of the Polyclada
—The nature of spiral cleavage — Definition of cell-lineage ami the nomenclature
employed — Miiller's larva in the development of Yuncjia and its metamorphosis —
The interpretation of Miiller's larva and the light which it throws on the
ancestral history of Platyhelminthes ... . Page 102

CHAPTER VI

NEMERTINEA

The development of Cerebratulus lacteus as a type of the Nemertinea — The Pilidium
larva and its metamorphosis — Experimental embryology of the Nemertinea — The
interpretation of the Pilidium larva and the light which it throws on the
ancestral history of Nemertinea .... Page 118

CHAPTER VII
ANNELIDA

Methods of preserving and mounting the eggs of Annelida— The development of
Polygordius append iculatus as a type of the Annelida: its cell - lineage : its
Trochophore larva and the metamorphosis- thereof — The Trochophore larva of
Polygordius lacteus and its metamorphosis — The development of various
Polychaeta — The development of the nephridia of Criodrilus — The development
of Ncphelis as a type of the Hirudinea — The development of Clepsine — The inter-
pretation of the Trochophore larva and the ancestry of the Annelida . Page 128

CHAPTER VIII
ARTHROPODA

The development of Pcripatus capensis as a type of the Prototracheata — The develop-
ment of Astacus as a type of the Crustacea — The formation of layers in Homarus,
Lucifer, and Euph.ausia as types of the Eucarida — The formation of layers in
Jlhjsis as a type of the Peracarida— The formation of layers in Polyphemus and
Jli'i/ttf/ripus as types of the Cladocera — The formation of layers in Lcpas as a type
of the Cirripedia — The larval history of Cyclops as a type of Crustacean larval
history : the Nauplius and Metanauplius larval stages — The larval history of
Phyllopoda : the Nauplius larva of Apus and Bmnchipus — The larval history of
Cirripedia : the Nauplius and Pupa stages — The larval history of Ostracoda —
The larval history of Euphausidacea and Penaeidea : the Nauplius, Protozoaea, and

CONTENTS xiii

Zoaea larval stages — The ancestral meaning of the Nauplius larva — The develop-
ment of the parasitic Copepod, Adheres ambloptitis, and the support which it gives
to the recapitulation theory of development — The Zoaea larva in Euphausidacea,
Penaeidea, Caridea, Anonmra, and Brachyura — Ancestral meaning of the Zoaea

larva The Mysis larval stage : its modification in the Loricata into the Phyllo-

soma larva : its modifications among the Crangonidae and Thalassinidae — The
Megalopa larval stage of Brachyura — The brephic stages in Anomura — The larval
history of Stomatopoda— The Metanauplius, Erichthoidina and Erichthus larval

stages Tlie Alima larva — The larval history of Port-union as a type of the

parasitic Isopoda — The development of Agelcna, a type of the Araclinida — The
development of Limulus : its Trilobite larva and the significance thereof— The
development of the Scorpion and of some other Araclinida — The development of
Pantopoda — The development of Tardigrada — The early development of Donacia
as a type of the embryonic development of Insecta — The early development of
Doryphora — The embryonic development of Blatta and the supposed origin of its
mid-gut epithelium — The development of the genital organs in Phyttodromia—
The formation of the embryonic membranes in the primitive Aptera (Lcpisma and
Machilis) — The metamorphosis of Galerucclla ulmi as type of the larval history of
Insecta — The development of the wings in Doryphora — The development of the
compound eye in Dytiscus — The metamorphosis in various families of Coleoptera,
Diptera, and Lepidoptera — The complicated metamorphosis of the Muscidae — The
meaning of metamorphosis as exemplified by observations on Bomlyx — The
development of Scolopendra as type of the Myriapoda — The development of Julus
— The ancestral history of Arthropoda . . . Page ] 69

CHAPTER IX

MOLLUSCA

I

The development of Patella as a type of the Mollusca — The metamorphoses of Acmaea,
Fissurclla, and Haliotis — Experiments on the eggs of Patella — The development
of Palndina as type for the formation of the internal organs of Gastropoda — The
development of Polyplacophora — Methods of preserving and staining the eggs of
Gastropoda— Various modes of the development of the velum in Gastropoda—
The larval kidneys of Gastropoda and their supposed homologies— The develop-
ment of Solenogastres — The development of Dentalium as type of the Scaphopoda—
Experiments on the eggs of Dentalium — The effect of cutting off the polar lobes of
the egg — The development of Dreissensia as a type of the Pelecypoda — The larval
development of the oyster — The development of Yoldia as a type of the Proto-
branchiata — The mode of development of heart and pericardium .in Cyclas — The
development of Unionidae— The Glochidium larva — The segmentation of the egg
of Sepia as a type of Cephalopod egg— The development of Loligo as type of the
Cephalopoda — The development of the eye of Cephalopoda— General considerations
on the ancestral history of the Mollusca .... Page 291

CHAPTER X

PODAXONIA

The development of Phascolosoma as type of the Sipunculoidea — The affinities ol
Podaxouia — The development of Sipunculus — The development of Phoronis:
various views as to its affinities . . . Page 372

xiv INVE11TEBKATA

CHAPTER XI
POLYZOA

The development of Membranipora as typo of the Polyzoa ectoprocta — The Cypho
nautes larva and its metamorphosis — Other types of larvae belonging to the
Polyzoa ectoprocta — The formation of buds in Polyzoa ectoprocta — The develop-
ment of Pedicellina cch'inata as a type of the Polyzoa entoprocta : its larva and its
peculiar metamorphosis — Ectoproct and Entoproct larvae compared — General con-
clusion as to the ancestral history of Polyzoa, Ectoprocta, and Entoprocta. Page 386

CHAPTER XII
BRACHIOPODA

The development of Terebratulina septcntrionalis as type of the Brachiopoda—
Affinities of the Brachiopoda as indicated by their development . Page 407

CHAPTER XIII
ROTIFERA

The development of Callidina russeola as a type of the Rotifera — The affinities of the
Rotifera . ... Page 418

CHAPTER XIV
CHAETOGNATHA

The development of Sacjitta bipunctata as a type of the Chaetognatlia— The ancestry
of the generative organs — The affinities of the Chaetognatlia . . Page 428

CHAPTER XV

NEMATODA

The development of Ascaris •incij/tloccphda as a type of the Nematoda — Methods of
obtaining, rearing, and preserving the eggs — The cell-lineage — The diminution
of chromatin — The formation of layers — The Rhabditis larva — The development
of T-giants and the conclusions as to the constitution of the egg-cytoplasm to be
deduced from them — The development of doubly-fertilized eggs and their bearing
on the caiises of diminution of the chromation — Experiments on the egg of
Ascaris — The affinities of the Nematoda .... Page 437

CHAPTER XVI
ECHINODERMATA

The development of Asterias as a type of the Asteroidea — Methods of obtaining the
eggs of Asterias — Methods of preserving and mounting the eggs and larvae of

CONTENTS xv

Eclunodermata generally — The formation of layers — The frequent presence of a
right madreporic pore — The Bipinnaria larva : its Brachiolaria phase and its
metamorphosis — The occasional presence of a right hydrocoele — The metamor-
phosis of Astropectinidae — The formation of organs in Asterina gibbosa — Peculiar-
ities in the development of Cribrella and tiol aster — Experiments on the eggs of
Asteroidea — Driesch's argument in favour of the existence of an entelechy—
Herbst's experiments in solution of sulphocyanide of potassium — The development
of Ophiothrix fragilis as a type of the Ophiuroidea — The Ophiopluteus larva
and its affinities with the Bipinnaria larva — The metamorphosis of the Ophio-
pluteus— The development of the calcareous skeleton and of the genital organs in
Amphiura squamata — The development of Ophiura brevispina — The development
of Echinus esculentus as a type of the Echinoidea — Methods of obtaining,
fertilizing, and rearing the eggs — The Echinopluteus larva and its affinities with
the Ophiopluteus larva — The metamorphosis of the Echinopluteus larva — The
ammotic cavity possibly originally a part of the larval stomodaeum — Peculiar
features in the development of Echinocijamus, Mellita, and Echinoeardium —
Experiments on the eggs of Echinoidea — -The results of hybridization : (1) between
dill'erent classes, (2) between different orders, (3) between different species — The
artificial parthenogenesis of eggs and the means of producing it — Effects of
separating the blastomeres of the developing egg and of cutting up the blastulae
—The effects of chemical substances on the development of the egg — The Lithium
larva and the explanation thereof — Formative stimuli — The development of
Synapta diyitata as a type of the Holothuroidea — The Auricularia larva : its
resemblances to the Bipinnaria larva — The metamorphosis of the Auricularia
larva — The pupal stage and its change into the adult Holothuroid — The formation
of the genital organs in Synapta vivipara and in Cucumaria glacial-is — The
development of Holothuria tubulosa — The development of Cucumaria planci— The
post-larval development of Antarctic species of Cucumaria — The development of
Antedon rosacea as a type of the Crinoidea — The formation of layers — The free-
swimming larva — The metamorphosis of this larva into the fixed Pentacrinoid
larva — The attainment of the adult form — Ancestral significance of the Echino-
derni larva — The Dipleurula ancestor of Echinodermata and its relation to the
Ctenophore-like ancestor of Annelida and Mollusca — The interpretation of Echino-
derm metamorphosis and the reason for the divergence of the Asteroid and
Grinoid stocks — The causes of the evolution of Ophiuroidea, Echinoidea, and
Holothuroidea ........ Page 456

CHAPTER XVII

PROTOCHORDATA

Meaning of the term Protochordata — The development of Balanoglossus davigerus as
a type of the Hemichorda — The development and metamorphosis of the New
England Tornaria larva — The metamorphosis of the Nassau Tornana larva —
The Tornaria larva of the Pacific coast — -The development of Dolichoglossus
koivalcvskii — The development of Dolichoylossus pusillus — The affinities of the
Hemichorda to Echinodermata — The development of Amphioxus lanceolxl//*
as a type of the Cephalochorda — -The process of gastrulation — The formation of
the coelom — The formation of the mouth and first gill-slits — The larva and its
primary gill -slits — The formation of the sclerotomes, nephridia, and genital
organs — The formation of the secondary gill-slits and the metamorphosis of iln
jarva — The evidence in favour of the affinity of Amphioxus with the Hemichorda

xvi INVEKTEBKATA

—The ancestral meaning of 'the asymmetry of the larva — The development of
Cynthia partita, as a type of the Urochorda — Its cell-lineage and the segregation
of coloured organ-forming substances — The process of gastrulation — The develop-
ment of the nervous system — The free-swimming larva of simple Ascidians and
its metamorphosis — The formation of heart, pericardium, and epicardium — The
formation of the stigmata — The development of the genital organs in Molgula—
Experiments on the eggs of simple Ascidians — Development of Molgula atupul-
loidcs — The Development of Ascidiae compositae — The development of Pyrosoma
as a type of the Ascidiae luciae — The Cyathozooid — The development of tialpa
as a type of the Thaliacea — The formation of the placenta — The development of
Doliolum — The development of buds in Urochorda — Stolonial budding— The
organogeny of the Blastozooid — The Ascidiozooids of Pyrosoma — The buds of tialfin
and of Doliolum — Pallial budding in the Botryllidae — Budding in Diplosomidae

—The reason for the different organogeny in the bud and in the larva — The
affinities of the Urochorda with the Cephalochorda . . . Page 568

CHAPTER XVIII

SUMMARY

Physiological explanation ot recapitulation — Evidence in favour of the possibility of
the inheritance of functional adaptations — Secondary modifications of the re-
capitulatory life - history — The effect of yolk and of maternal secretions — The
modus operandi of organ-forming substances — Sketch of the ancestral history of
Metazoa ......... Page 649

ERRATA

Page 9, line 38, for "cell sap" read "cell and sap."

,, 61, lines 5 and 6, for "medusa <S'. apicata" read "medusa of >S'. apicata."
,, 125, line 22, for "first nucleus" read " nuclear matter of the sperm head."
,, 126, line 4, for " broken in two " read " broken into."

ILLUSTRATIONS

1. Eight views of the maturation of the male cells of Lepidosircn paradoxa . 5

2. Nine stages in the transformation of a spermatic! into a spermatozoon . 8

3. Four stages in the maturation and fertilization of the egg of Orepidula

plana ......... 10

4. Two stages in the first division of the fertilized egg of Crepidula plaim . 11

5. Polar view of the first maturation division of the male germ cells of Alydus

pilosulus in order to show tetrads ...... 12

Second maturation division of the male germ cells of Protenor belfrayci . 14
Second maturation division of the male germ cells of Euschistus variolaris . 14
The larva and adult female of Porlunion maenadis . . . .23

The stalked larva and adult form of Antedon multispina . . .24

The larva and just-metamorphosed form of the Plaice (Pleuronectes platcssa] 25
Unripe egg of Limulus polyphemus. An example of a centrolecithal egg . 27
The ripe egg of Stront/ylocentrotus lividus. An example of an alecithal egg 27
Two stages in the segmentation of the egg of Sycandra raphanus . . 38

View of the embryo of Grantia labyrinthica in the blastula stage lying in

the embryonic chamber of the mother . . . . .39

View of the embryo of Grantia labyrinthica in a later stage of development

than that represented in Fig. 14 . . . . . .39

Section of a portion of Grantia labyrinthica . . . . .40

The Amphiblastula larva of Grantia labyrinthica ' . . . .40

Two stages in the fixation of the larva of Sycandra raphanus . . 41

An early stage in the metamorphosis of the Ascon stage of Syrt/m/ri/

raphanus into the adult ....... 41

A late stage in the metamorphosis of the Ascon stage of Sycandra wtyhanus

into the adult condition ....... 42

Longitudinal sections through the free-swimming larva ofOsat-i-fffa luln/lnrix

in two stages of its development and its fixation . . . .44

Seven stages in the metamorphosis and fixation of the larva and growth of

the young sponge of Plakina monolopha . . . . .45

Two sections of the body-wall of the larva of Plakina monolopha, to show

the distinction between archaeocytes and mesenchyme . . .46

Longitudinal section through the Amphiblastula larva of Esperia lorcnzi . 46
Longitudinal sections of the Amphiblastula larva, the just-fixed larva, and

the young sponge of Leucosolenia variabilis . . . .48

Section through a gemmule-beariug individual of Ephydatia blembinyia . 49
Three stages in the formation of the gemmules of Ephydatia blembinyia . 50
Two methods of formation of the blastula in Tulularia mescmbryanthcmum 55
Formation of endoderm in Tubidaria mescmbryanthcmu/n . . 55

xvii //

xviii INVEETEBEATA

FIG. i-AGli

30. Section of embryo of Tubularia mesembryanthemum showing the formation

of the aboral tentacles ....... 56

31. Five views of external features of different stages in the development of the

embryo of Ttibularia indivisa ...... 56

32. Two gonophores of Tubularia indivisa with developing embryos inside . 57

33. Stages in the development of the Actinula larva of Tubularia indivisa . 57

34. Three longitudinal sections through the developing gonophore of Tubularia

mesembryanthemum. ....... 58

35. Four transverse sections through the developing gonophore of Tubularia

mesembryanthemum . . . . . . . .59

36. Longitudinal section through very young gonophore -bud of Tubularia

mesembryanthemum to show the origin of the genital cells . . 59

37. Four stages in the development of the planula of Clytia . . 60

38. Three stages in growth of the fixed planula of Clytia . . 60

39. A young colony of Clytia reared from a planula in the aquarium . . 61

40. Two longitudinal sections through the developing medusa of Podocoryne

carnea ......... 62

41. Four transverse sections through the developing medusa of Podoeoryue

carnea in order to show formation of circular canal and endoderm lamella 63

42. Two longitudinal sections through the developing gonophore of Clara

squamata ......... 64

43. Three stages in the development of a Siphonopliore (Cystalia monogastrica) 65

44. Embryo of a Geryonid ( Carmarina fungiformis) in which endoderm cells

are being budded oft' . . . . . . .67

45. Early stages in the development of Aurelia aurita . . . .68

46. The fixation of the free-swimming larva of A urelia aurita . . .68

47. Two longitudinal sections through two Hydra-tubae of different ages . 69

48. Two transverse sections through a Hydra-tuba with four tentacles . . 70

49. A, a Hydra-tuba with eight tentacles. 13, longitudinal section of a part of

a similar specimen in order to show origin of septal funnels . . 71

50. Oral view of Hydra-tuba with twenty tentacles. (The tentacles are repre-

sented as cut off) . . . . . . . .71

51. Two horizontal sections through the upper part of a Hydra-tuba, about as

old as that represented in Fig. 50, to show the formation of the ostiuni
connecting the stomach pockets ...... 72

52. Two stages in the ttrobilization of the Scyphistoma of Aurelia aurita . 73

53. A strobilized Scyphistoma of Aurelia aurita . . . . .74

54. An Ephyra larva of Aurelia aurita just after liberation from the strobilized

Scyphistoma ........ 74

55. Longitudinal section through the sense organ of a young Ephyra . . 75

56. Three stages in the development of the Ephyra larva into the adult Aurelia, 75

57. An egg of Urticina crassicornis dividing into sixteen blastomeres . . 77

58. Four stages in the development of the egg of Urticina crassicornis as seen

in longitudinal sections ....... 78

59. Two stages in the development of the larva of Urticina crassicornis . 79

60. Two transverse sections through a larva of Urticina crassicornis in order

to show the formation of mesenteries . . . . .80

61. Transverse section through a larva of Urticina crassicornis in which the

tentacles have just been developed . . . . . • . 81

62. Longitudinal section through the larva of Ayaricia ayaricitcs in order to

show the ectodermal origin of the mesenterial filament . . 82

63. Stages in the development of the larva of Actinia equina . . .84

64. The Arachnactis larva of Cercantkus mcmbranaccus . 85

ILLUSTKAT10NS xix

65. The Zoanthina larva of a Zoantharian . . 86

66. Transverse sections of two types of Actinozoan larvae . . .86

67. Young living Caryophyllia cyathus, seen from above. The calcareous

skeleton shows through the transparent tissue . . . .87

68. Five stages in the development of the skeleton of Caryophyliiu, ci/nl/nts . 88

69. Side view of the segmenting egg of a Ctenophore (Oallianira Inal/i/n} . 89

70. Two views of the developing egg of Beroe ovata, seen from above . . 90

71. Oral and aboral views of the embryo of Beroe ovata in a later stage of

development . . . • . . . . .90

72. Illustrating the origin and fate of the so-called mesoderm in a (Jteiiophore

embryo (Collianira Malata) ...... 91

73. Optical section of embryo of Beroe. forskalii showing the beginning of the

endodermal cavities ....... 92

74. Optical section of embryo of Beroe forskiilii in a later stage of development,

with a hollow endodermal sac ...... 92

75. Two optical sections through the embryo of Beroe forskalii . . .93

76. Larva of Beroe forskalii four days old, viewed from "stomach-plane " . 93

77. Part of apical region of larva of Beroe forskalii, viewed from stomach-plane . 9-4

78. The free-swimming larva ofCallianira Malata, viewed from the stomach-plane 95

79. An embryo of Beroe ovata with four ribs and two endodermal pouches, and

a small extra third pouch ; obtained by isolating one of the first two
blastomeres of Beroe ovata ....... 97

80. Developing egg of Planocera inquiiina. Eight-cell stage, viewed from

animal pole ......... 105

81. Developing egg of Planocera inquiiina. Sixteen-cell stage, viewed from the

animal pole ......... 105

82. Developing egg of Planocera inquiiina. Thirty-two-cell stage, viewed from

vegetative pole ........ 107

83. Optical section of the developing egg of Planocera inqitiii/tx, viewed from

posterior pole ..... . 108

84. Diagrammatic frontal section through the egg of Planocera inqnili/ia at a

later stage of development than that represented in Fig. 83 . . 109

85. Developing egg of Planocera inquiiina in a late stage of segmentation, viewed

from animal pole ........ HO

86. Three longitudinal sections through developing embryos of PtoioceroMigwJmo! Ill

87. A, dorsal, and B, ventral views of the free-swimming larva of Yuncjia

aurantiaca . . . . . . . . .112

88. Lateral view of the free-swimming larva of Yumjia aurantiucu . . 112

89. A, dorsal, and B, ventral views of larva of Yu-iujla aurantiaca in which

metamorphosis is beginning . . . . . .113

90. A, dorsal, and B, ventral views of larva of Yiunjia aurantiaca in which

metamorphosis is almost complete ..... 113

91. Median sagittal longitudinal section through larva of Yunyia auratitiaca . 114

92. Median sagittal section through a young Polyclade worm (Yungia aur-

antiaca) just after its metamorphosis ..... 115

93. Two stages in the segmentation of the egg of Ccrebratulus lacteus, viewed

from the side ... . .119

94. The young gastrula of Cerebratulus laetcus . . . . .120

95. Two stages in the development of the Pilidium larva of Cerebratulus lactcus

showing the development of mesenchyme into muscles. A, earlier stage.

B, later stage ........ 121

96. Two views of advanced Pilidium larva of L'crcbrattthis lactcus in order to

show the development of the muscles ..... 121

xx INVEKTEBKATA

FIG. 1'AOE

97. A Pilidium larva shortly before its metamorphosis .... 122

98. Longitudinal section through a Pilidium larva of about the age of that

represented in Fig. 97 ....... 123

99. Two stages in the development of the Nemertine rudiment within the

Pilidium, viewed from above ..... 124

100. The Trochophore larva of Poly/jordius, viewed from the side . . 130

101. Stages in development of the blastula of Polygordius seen in optical

longitudinal section ...... 132

102. Dorsal view of upper hemisphere of egg of Polijgordius, in which seventy-

six cells have been formed . . . . . . .134

103. Three stages in the segmentation of the lower or vegetative surface of the

egg of Polygordius ....... 136, 137

104. Four views of the vegetative pole of the developing egg of Polygordius in

order to show the processes of gastrulation and of the formation and
closure of the blastopore ....... 141

105. Four diagrammatic transverse sections of lower part of young Trochophore

larva to show the mode of closure of blastopore .... 142

106. Optical sagittal section of young Trochophore after gastrulation is complete 143

107. Later stage in the development of Polygordius appendiculatus, in which

the " worm-body " is being formed by the growth of the trunk blastema . 145

108. Longitudinal sections of stage represented in preceding figure in order

to show details ........ 146

109. Two sections of the anterior part of a larva of Polygordius appendiculatus

in order to show the changes supervening on metamorphosis . . 149

110. Polygordius appendiculatus immediately after metamorphosis . . 150

111. Longitudinal sections of anterior portion of Polygordius appendiculatus

immediately after metamorphosis in order to show details . . 151

112. Late larva of Polygordius lactcus in optical frontal section . . .152

113. Figure illustrating the origin of the mother cells of the adult mesoderm in

Eupomatus , . . . . . . . .154

114. Diagrammatic sagittal section of fully-grown Trochophore larva of Eupo-

matus in order to show the relative position of the protonephridia and of

the coelomic rudiment '....... 155

115. Stage in the segmentation of the egg of Nereis limbata, viewed from above,

showing a laeotropic spiral cleavage of the egg .... 155

116. The free-swimming larva of Nereis limbata, three days old. A typical

" Polytrochal " larva ....... 156

117. Transverse section through the ventral part of an embryo of Criodrilus

lacuum . . . . . . . . .158

118. Two longitudinal sections through the ventral portion of an embryo of

Criodrilus lacuum . , . , . . . .159

119. Two longitudinal sections of embryos of Nephelis vulgaris . . . 160

120. A fairly advanced embryo of Cosine (Glossiphonia], seen from behind . 161

121. Hinder view of a well-developed larva of Nephelis vulgaris . . 162

122. Larva of Nephelis vulgaris, viewed from the side . ... . 162

123. Stages in the segmentation and the gastrulation of the egg of Peripatus

capcnsis ........ . 170

124. Stages in the division of the blastopore and the formation of the mesoderm

of Peripatus capensis ....... 172

125. Diagrammatic transverse sections through the bodies of embryos of Peri-

patus capcnsis of various ages in order to illustrate the mutual relation-
ships of haemocoele (primary body-cavity) and coelom (secondary body-
cavity) ......... 173

ILLUSTRATIONS xxi

FIO. PAGE

126. The formation of the appendages in the embryo of Peripatus c(tj>i:iisis . 175

127. Two sections through the developing egg of Astacus . . 179

128. Sagittal section through the blastula of Astacus fluviatilis in order to

show the primary yolk pyramids ...... 180

129. Ventral view of an embryo of Astacus fluviatilis, the gastrula stage, in

order to show the ventral plate . . . . . .181

130. Sagittal section through a portion of the embryo of Astacas fluviatilis in

order to show the imagination of the endodermic rudiment . .182

131. Two sagittal sections through developing eggs of Astacus fluviatilis in

order to show the development of the endoderm .... 182

132. The " Nauplius " stage in the development of Astacus fluviatilis, viewed

from the ventral side . . . . . . .184

133. Three transverse sections through the developing nerve cord of Astufux

fluviatilis . . . . . . . . .185

134. Two views of developing eggs of Astacus fluviatilis from the ventral surface 186

135. Transverse section through the region of the heart in an embryo of

Astacus fluviatilis in about the same stage as that represented in Fig.

134 B ...... 187

136. Longitudinal section through advanced embryo of Astacus fluviatilis

parallel to the sagittal direction but to one side of the middle line . 187

137. Advanced embryo of Astacus fluviatilis, viewed from the ventral side. The

abdomen and hinder part of the thorax are cut off and spread out
separately ......... 188

138. Two ommatidia from the eye of a newly-hatched Astacus fluviatilis in

longitudinal section ....... 188

139. Two sagittal sections through advanced embryos of Astacus fluviatilis . 190

140. Portions of two sagittal sections through developing eggs of Homarus

americanus ......... 191

141. Sections through the developing egg of Mysis chamaeleo . . 192

142. Stages in the development of the egg of Polyphemus pcdiculus . . 193

143. Four sagittal sections through the developing eggs of Lepas anatifera in

different stages of development ...... 195

144. The Nauplius larva of Cyclops cantliocarnoidcs from the ventral surface . 197

145. Three stages in the further development of the larva of Cyclops . . 198

146. Two types of Nauplius larva ...... 199

147. The " Cypris " larva or Pupa of Lepas fascicularis, seen from the wide . 200

148. The fixation of the Cypris larva of Lepas fascicularis . 201

149. The Nauplius larva of Cypris ovum, . . . 202

150. The Protozoaea larva of Nyctiphancs australis 203

151. Dorsal and ventral views of the " Copepodid " larva of Adheres ambloplitis 205

152. Dorsal and lateral views of the just-fixed female of Adheres amblopltiis . 206

153. Lateral view of female Adheres ambloplitis after the adult characteristics

have been attained ..... 206

154. Enlarged view of gnathites and lips of female Adheres aw/i/nfJit/s, seen

from the side ..... 207

155. " Calyptopis " Zoaea of Nydiphanes aiistralis, lateral view . 208

156. Zoaea larva of Penacus, ventral view . . . 209

157. Zoaea larva of Crane/on vulgaris, lateral view

158. Zoaea larva of Porccllana longicornia after the lirst moult . 211

159. Zoaea larva of the Crab Xantho

160. " Mysis " larva of Homarus amcricanus, lateral view

161. " Phyllosoma " larva of Palinurus vulgaris, ventral view . 214
:< Mysis " larva of Cranrjon allinauni, lateral view .

xxii INVEKTEBKATA

FIG. l>A("iK

163. " Megalopa " larva of the Crab Pilumnus, dorsal view . . . 215

164. Two views of first post-larval stage of Eupagurus bcrnhardi, corresponding

to the Megalopa stage of Brachyura . . 216

165. Two stages in the development of a Stomatopod larva . . .217

166. Two later larvae of Stomatopoda . . .218

167. Larva and adult female of Portunion maenadis . . .219

168. Adult female of Portunion maenadis with appendages dissected out . 220

169. Three stages in the segmentation of the egg of Agelena . . . 222

170. Surface views of the developing egg of Agelena lalyrinthica, showing the

primitive streak and the primitive cumulus

171. Section through the primitive streak of Agelena to illustrate the forma-

tion of the germ layers . . 224

172. Two views of embryo of Agelena at the period of maximum extension of

the ventral plate (i.e. before reversion has begun). The coelomic cavities

are seen by transparence and are represented by lighter shading . 225

173. Two sagittal sections through embryo of Agelena of different ages, but

previous to reversion . . • 226

174. A portion of a sagittal section of Agelena lalyrinthica . 227

175. Two views of embryos of Agelena undergoing reversion . . 227

176. Transverse sections through the heart of Agelena lalyrinthica in two

stages of development ....

177. The embryo of Agelena when reversion is complete .

178. Longitudinal section through part of the abdomen of Agelena lalyrinthica

in order to show the origin of the genital organs . . 229

179. Two sections through the developing stercoral pocket and ilalpighian tubes

of Agelena lalyrinthica ....... 230

180. Sagittal section through the hinder part of the abdomen of Agelena

lalyrinthica to show the hinder part of the mid-gut developing in
connection with the stercoral pocket . . • 231

181. Longitudinal section through the abdominal appendages of an embryo of

Agelena lalyrinthica in order to show the origin of the lung book . 231

182. Surface views of the cut-off abdomen of three embryos of Agelena

lulujrinthica of different ages in order to show the modifications under-
gone by the abdominal appendages ..... 232

183. The condition of the brain in the embryo of Agelena after reversion has

taken place ..... 233

184. Sections through the developing eyes of Agelena . . . 234

185. Two sagittal sections through embryos of the spider Thcridion maculatum

in two succeeding stages of development ..... 234

186. Horizontal section through abdomen of an advanced embryo of Agelena

lalyrinthica in order to show the division of the yolk into lobes by septa 235

187. Ventral view of an embryo of Limulus lonyispina, twenty-one days old . 237

188. The Trilobite larva of Limulus .... .238

189. Two transverse sections through the " germinal disc," or developing area, of

the egg of the Scorpion Euscorpius carpathicus in two stages of development 239

190. Ventral view of embryo of the Scorpion Euscorpius carpathicus showing

segments and appendages ..... . 239

191. Larva of Ascorhynchus minutus . . . 242

192. Dorsal view (optical frontal section) of the embryo of Macrobiotus . 243

193. Portion of a sagittal section through the developing egg of Doryphora

(Lcptinutarsa] deccmlincata before the formation of the blastoderm . 246

194. Surface view of the egg of Donacia crassipcs at the conclusion of blastoderm

formation .... 247

ILLUSTRATIONS xxiii

*'10' PACE

195. Section through the dorsal part of a developing egg of Donacia crassi/"'*

in order to show the primitive dorsal organ ... . . 247

196. Diagrams showing the relations sustained to one another by amnion, serosa,

and embryonic area in three succesive stages of the development ofDoiw<-;<i
crassipcs ....... .248

197. Diagrams to illustrate the formation of the posterior amniotic fold in the

egg of Donacia crass? 'pcs . . . . . . .219

198. Two transverse sections through the gastral groove of the egg of Donacia

crassipcs after it is closed ....... 250

199. Three surface views of the embryo of Donacia crassipcs at a stage when

the germinal streak begins to show division into segments . . 251

200. Longitudinal section through the abdominal appendage of the embryo of

Donacia crassipes in order to show its glandular character . . 252

201. Diagram of a longitudinal section parallel to the sagittal plane, but some-

what lateral, through the embryo of Donacia crassipes in order to show

the coelomic sacs ........ 254

202. Sagittal sections through the stomodaeum and proctodaeum of Donacia

crassipcs . . . . . . . . .255

203. Diagrammatic representation of mid-gut of the embryo of Donacia crassijjcs

showing its lateral pouches ...... 255

204. Two transverse sections through embryos of Donacia, crassipcs of different

ages, in order to show the modifications undergone by the coelomic sacs . 256

205. Two diagrammatic sagittal sections through the egg of Periplaneta

oricntalis in two stages of development ..... 259

206. The "grub" of Doryphora (Lcptinotarsa} dccemlineata in the third instar,

from the side ........ 260

207. Longitudinal section through the embryonic area of an embryo of

Phyllodromia gcrmanica ....... 263

208. Transverse sections through three embryos of Phyllodromia gcrmanica at

three stages of development in order to show the development of the
coelomic sacs, the fat body and the generative organs . . . 264

209. The rudiment of the female genital organs of Phyllodnniun germanica

reconstructed from sagittal sections ..... 264

210. Two views of the egg Lepisma saccharina in different states of develop-

ment ......... 265

211. Two diagrammatic lateral views through the egg of Machilis altcrnata in

different stages of development ...... 266

212. Diagram of the anatomy of the larva of Galcrucclla ulmi . . . 267

213. Portions of sections through the valve separating stomodaeum from mid-

gut in the larva of Galcrucclla ulmi ..... 269

214. Sections of the epithelium of the mid-gut in the pupa of Galcrucclla nlnii

showing the changes undergone by this tissue at the metamorphosis

into the adult condition ....... '270

215. Portions of the Malpighian tubes of a larva and a pupa of Galcrucclla ulmi 270

216. Portion of the abdominal muscles of the larva of Galcrucclla ulmi under-

going histolysis ........ 271

217. Diagrammatic sections through the imaginal disc of a wing in various

stages of development showing how the wings develop in various groups

of insects ......... '27'2

JM8. Two views of the head of the larva of Dijtiscus marcjinalis in two stages

of development ..... . 273

219. Longitudinal section through the simple eye of larva of Dijtiscus manjinalis

parallel to its shortest diameter .... . 274

xxiv INVEKTEBBATA

FTC. I'AOK

220. Lateral views of the head of the larva of Dytiscus marcjinalis in three

stages of development in order to show the gradual growth of the rudi-
ment of the compound eye .... 274

221. Two stages in the development of the compound eye of Dytiscus marginalis

as seen in longitudinal section .... 2/5

222. A small portion of the adult compound eye of Dytiscus marginali as seen

in longitudinal section ... 2/6

223. Diagrams illustrating the metamorphosis of Musca vomitoria . . 277

224. Two diagrams illustrating the metamorphosis of the head of Musca

vomitoria . . . . • • • • .2/8

225. Ventral view of the embryonic area in a developing egg of Scolopcndra

cingulata ......

226. Development of Patella coerulca. Eight-cell stage showing the spindles

preparatory to the formation of the 16-cell stage . . 293

227. Two stages in the development of the upper hemisphere of the embryo of

Patella coerulea, viewed from above . . . 294

228. Stage in the development of the embryo of Patella coerulea, viewed from

the vegetative pole of the egg, showing the first division of the third
quartette and the beginning of bilateral symmetry as seen in the
direction of the spindles in 3c and 3d • 295

229. Two stages in the gastrulation of Patella coerulea in optical longitudinal

section ....... • 296

230. The "Ctenophore" stage in the development of Patella coerulca. Seen

from above ...... 296

231. View of the upper hemisphere of an embryo of Patella coerulea just before

hatching ....... .297

232. Lateral view of a late embryo of Patella coerulca showing the mode of

completion of the pro to trochal girdle . . . 297

233. Three diagrams of sagittal sections of the early larva of Patella coerulca

in order to illustrate the shift of the blastopore and the formation of the
stomodaeum ..... 298

234. Lateral view of young Trochophore larva of Patella coerulea . . 299

235. Ventral views of two stages in the development of the Trochophore larva

of Patella coerulea ........ 300

236. Side view of a Veliger larva of Patella coerulca before torsion has taken place 301

237. Side view of a Veliger larva of Patella coerulca after torsion has taken

place .302

238. Frontal section of a Veliger larva of Patella coerulca in order to show the

mesodermic bands ..... . 303

239. Frontal section through the pre-trochal region of an old Veliger larva of

Patella coerulca ........ 303

240. Two views of advanced stages of development of Acmaea virginca . . 304

241. Three views of the just -metamorphosed Acmaea mrginca in order to

show the formation of the adult shell and the loss of the larval shell . 305

242. Two views of the young Haliotis tiolcrculata in order to show the forma-

tion of the adult shell ..... .306

243. Illustrating the results obtained by separating the blastomeres of the

developing egg of Patella coerulca .... . 308

244. Vertical section of the gastrula of Paludina vivipara . . 310

245. Formation of the coelom in Paludina vivipara . . .311

246. Optical frontal section of an embryo of Paludina vivipara a little older

than those represented in Fig. 245 . . . 311

247. Two stages in the formation of the pericardium of Paludina vivipara . 312

ILLUSTRATIONS xxv

Fin.

248. Horizontal section through the visceral hump of an older embryo of

Paludina vivipara than that represented in Fig. 247 in order to show the
formation of the kidneys and the heart ..... 313

249. Illustrating the development of the ureters of Paludina vivipara and their

relation to the kidneys ....... 314

250. Two embryos of Palvdina vivipara, viewed from the right side, in order to

show the origin of the sense-organs and the beginning of torsion . . 316

251. Just hatched Paludina vivipara, seen from the left side and viewed as a

transparent object ........ 317

252. Transverse sections through the visceral humps of two embryos of Paludina

vivipara of different ages in order to illustrate the torsion of the organs,
the development of the genital organs and their connexion with the right
kidney, and the lengthening of the visceral hump associated with an
increase in length of the liver ...... 318

253. Apical region of an embryo of Cr<'pnlnla- showing the Molluscan cross in

a late stage of development ...... 322

254. Embryo of Limnaca staynalis, viewed from right side as a transparent

object, in order to show the larval kidney ..... 324

255. Vertical sections of the eggs of Dentalium before and after fertilization in

order to show the flow of cytoplasmic substances .... 326

256. Stages in the cleavage of the egg of Dentalium .... 327

257. Further stages in the cleavage of the egg of Dentalium . . . 328

258. The Trochophore larva of Dentalium, twenty-six hours after fertilization . 329

259. Transverse section of the Trochophore larva of Dentalium in the region of

the prototroch ........ 329

260. Veliger larvae of Dentalium ....... 330

261. Larvae resulting from the development of eggs of Dentalium from which

the polar lobe has been removed . . . . . .331

262. Vertical section of a larva of Dentalium developed from egg from which

the first polar lobe had been removed in order to show the absence of
mesoderm . . . . . . . . .331

263. Longitudinal section of the 2-cell stage of Dreissensia polymorpha in order

to show the blastocoele ....... 333

264. Stages in the cleavage of the egg of Dreissensia put [imorpha . . 334

265. Sagittal sections of embryos of Dreissensia polymorpha showing the process

of gastrulation and of the formation of the shell gland . . . 336

266. Young Trochophore larva of Dreissensia polymorpha, seen from the ventral

side .......... 337

267. Sagittal section through a young Trochophore larva of Dreissensia poly-

•iniirpha ......... 338

268. Transverse section of the ventral portion of a young Veliger larva of

Dreissensia polymorpha in order to show the origin of the mantle-groove
and of the pedal ganglia .......

269. Young Veliger larva of Dreissensia polymorpha, seen from the side' . 339

270. Young Veliger larva of Dreissensia iwlymorphu, seen from the ventral

surface ......... 340

271. Older Veliger larva of Dreissensia polymorpha, seen from the side. This

stage is the one which immediately precedes the metamorphosis .

272. Transverse section through the dorsal region of an old VeligtT larva of

Dreissensia polymorpha in order to show the differentiation of the
pericardium and the kidneys ....

273. Sections through the cerebral pit of Veliger larvae of Dreissensiii. /<"///-

tnorpha ........ 343

xxvi INVERTEBEATA

FIO. I'/VIE

274. Horizontal section through the anterior portion of an old Veliger larva of

Dreisscnsia polymorpha in order to show the differentiation of the
cerebral ganglia from the cerebral pit ..... 344

275. Side views of two young specimens of Drcissensia polymorpha after the

metamorphosis has taken place ...... 345

276. Horizontal sections through the anterior portions of three just metamor-

phosed specimens of Dreissensia polymorpha in order to show the trans-
formation of the cerebral pit into the labial palps .... 346

277. Diagrammatic transverse sections of young specimens of Dreisscnsia poly-

morpha in order to illustrate the development of the kidney . . 347

278. Transverse section through a young Drcissensia polymorpka in order to

show the origin of the genital organs ..... 348

279. The late Veliger larva of Ostrea virginiana, viewed from the side . . 349

280. The Veliger larva of Yoldia limatula, about three days old . . 350

281. Longitudinal sagittal section through the Veliger larva of Yoldia limulata,

three days old ........ 350

282. Diagrams illustrating the development of the pericardium in Cyclas and

Drcissensia ......... 351

283. Glochidium larva of Margaritana with widely opened valves, viewed as a

transparent object from the dorsal surface ..... 352

284. Transverse section of a Glocliidium larva of Unio which is already fixed

in the tissues of its host ....... 353

285. Segmenting egg (32-cell stage) of Sepia officinalis, viewed from the animal

pole .... ..... 355

286. A portion of the margin of the blastoderm of the egg of Sepia officinalis

at the conclusion of the process of segmentation in order to show the
transformation of the blastocones into cells of the yolk-membrane . 356

287. Two sections through the edge of the blastoderm of Sepia officinalis in

different stages of development in order to illustrate the development

of the lower layer cells ....... 357

288. Two early embryos of Loligo vulgaris ..... 357

289. Embryo of Loligo vulgaris, seen from the posterior side at the conclusion of

the period of development, termed by Faussek Stage I. . . . 358

290. Two sagittal sections of early embryos of Loligo vulgaris in order to

illustrate the first formation of organs ..... 359

291. Embryo of Loligo vulgaris, seen from the side and behind, in order to

illustrate the development of the ganglia. The embryo is younger than

that represented in Fig. 289 ...... 360

292. Embryo of Loligo vulgaris in the stage termed by Faussek Stage 2, when

the embryo begins to be grooved off from the yolk-sac ; posterior view . 360

293. Sagittal sections of two embryos of Loligo vulgaris to illustrate the forma-

tion of internal organs ..... .361

294. Two diagrammatic transverse sections through a young embryo of Loli<j«

vulgaris in order to illustrate the origin of the coeloni and the blood
cavities ..... ... 362

295. Diagrams of three transverse sections through an embryo of Luliijo vulgaris

much older than that represented in Fig. 294 . . . 363

296. Embryo of Loligo vulgaris at the period when the funnel is formed, viewed

from behind ........ 364

297. Transverse sections of embryos of young cuttle-fishiillustrating two stages

in the development of the genital organs ... . 365

298. Two early stages in the development of the eye of Loligo vulgaris, seen in

transverse section . • • 366

ILLUSTRATIONS xxvii

FIG. I'A'.i:

299. Sections through the developing eyes of young cuttle-fish to show the

development of the lens ....... 366

300. Transverse section of the eye of a nearly ripe embryo of Sepia ojficinalis . 367

301. Early segmentation stages of the egg of Phascolosoma gouldii . . 373

302. Later stage in the segmentation of the egg of Phascolosoma gouldii, viewed

from the posterior aspect ....... 374

303. Two views of the apical region of the segmenting egg of Phascolosoma

vitlgare ......... 374

304. Nearly sagittal section of an embryo of Phascolosoma vulgare at the stage

when gastrulation is beginning ...... 375

305. A Trochophore larva of Phascolosoma cii/i/n-r>\ a little more than thirty-six

hours old ......... 377

306. Nearly sagittal sections through metamorphosing Trochophore larvae

of Phascolosoma ........ 378

307. Young specimens of Phascolosoma gouldii after the metamorphosis . 379

308. Lateral view of the Actinotrocha larva of Phoronis .... 381

309. Diagrammatic frontal section of the Actinotrocha larva of Phoronis (spl)

captured near Ceylon .......

310. Longitudinal horizontal section of the embryo of an Australian species of

Phoronis ....... .382

311. Three stages in the metamorphosis of the Actinotrocha larva of Phoronis,

seen from the side ........ 384

312. Early stages in the development of the egg of Mei)ibranipvra pilosa . 388

313. The development of the larva of Mcmbi-anipora pilosa . . . 389

314. Median sagittal section of the fully-grown Cyphonautes larva of Membrani-

pora pilosa ......... 391

315. Sections through fixed and metamorphosing larvae of Alcmbranipora

pilosa ......... 393

316. Two degenerate types of larvae of Ectoproct Polyzoa . . . 395

317. Stages in the development of the bud of Bucjula avicularia . . 397

318. Early stages in the development of the egg of Pcdicellina cchinata . 399

319. Nearly sagittal section lying to the right of the median plane through the

embryo of Pcdicellina cchinata . . . . 401

320. Optical sagittal section of the free-swimming larva of Pcdicellina cchinata 402

321. Median sagittal sections through two fixed and metamorphosing larvae of

Pcdicellina cchinata ....... 404

322. Optical sections of early embryos of Tcrcbratulina scptcntrionalis . . 408

323. Later embryos of Tcrcbratulina septentrionalis seen from the side (in

optical section) ....... 409

324. Dorsal and ventral views of larva of Tcrcbratulina septentrionalis . . 410

325. Lateral view of a larva of Tcrcbratulina scptcntrionalis . . 411

326. Frontal and sagittal sections of the larva of Tcrcbratulina septentrionalis 412

327. Two larvae of Tcrcbratulina septentrionalis just before and at the time of

fixation ....... 413

328. Two young Tcrcbratulina septentrionalis immediately after the meta-

morphosis ........ 414

329. Young Tcrcbratulina septentrionalis some little time after metamorphosis,

viewed from the dorsal surface ..... 415

330. Early stages in the segmentation of the egg of <.'«!li<Jiint. /'usscofa . 419

331. Further stages in the segmentation of the egg of I'uHiiliuii russeolu . 420

332. Sixteen-cell stage in the segmentation of the egg of C«llitliim russi nfn . r_'l

333. Two views of embryos of CaJlidina russcota showing the process of

gastrulation . 422

xxviii INVEKTEBBATA

FIG. PAGE

334. Optical sagittal sections of two embryos of Callidina russeola after the

process of gastrulation has been completed .... 423

335. Ventral view of embryo of Callidina russeola somewhat older than

those represented in Fig. 334 ...... 424

336. Optical sagittal sections through two late embryos of Callidina russeola

in order to show the formation of organs ..... 425

337. Ventral views of two embryos of Callidina russeola at a stage not long

before hatching ........ 426

338. Optical sections of early embryos of Sagitta bipunctata . . . 429

339. Cross section of the blastula of Sagitta Mpunctata in the 16-cell stage

showing the determination of the mother cell of the genital organs . 430

340. Optical section of older embryo of Sagitta Mpunctata showing the forma-

tion of the " head cavities " and of the stomodaeum . . . 431

341. Ventral view of the larva of Sagitta enflata on the fourth day after hatching,

in order to show the origin of the nervous system and the separation of

the trunk coelom from the tail coelom ..... 432

342. The 2-cell stage of the egg of Ascaris megalocephala (monovalens) when

the spindles for the 4-cell stage are being formed, showing the diminution

of the chromatin ........ 440

343. Early stages in the segmentation of the egg of Ascaris mcgaloccphala . 441

344. The 12-cell stage of the segmentation of the egg of Ascaris megalocephala,

seen from the left and the right sides respectively, in order to show the
rearrangement of the daughters of the cell AB . . . 442

345. Dorsal view of the segmenting egg of Ascaris megalocephala in the 20-cell

stage ......... 442

346. Ventral view of the segmenting egg of Ascaris megalocephala in the 24-cell

stage ......... 442

347. Dorsal view of the segmenting egg of Ascaris megalocephala in the 102-cell

stage ......... 443

348. Optical median sagittal section through the blastula of Ascaris megalo-

cephala at the time that the process of gastrulation is commencing . 444

349. Segmenting egg of Ascaris megalocepltala in the 102-cell stage, seen from

beneath ......... 445

350. Sagittal sections through three embryos of Ascaris megalocephala in

order to show the invagination of the genital cells and of the stomo-
daeal rudiment ........ 446

351. Transverse section of embryo of Ascaris megalocephala in order to show

the invagination of the anterior mesoderm cells and of the mother cells

of the genital organs . . . . • • 447

352. A " T-giant " of Ascaris megalocephala, seen from the leftside . 449

353. Two diagrams of the 4-cell stage in the development of the egg of Ascaris

megalocephala in order to show the cytoplasmic zones which Zur Strassen
assumes to exist in the blastomeres . . . 450

354. The stage corresponding to the 4-cell stage in the development of the

normal egg which occurs in the development of the three types of doubly
fertilized eggs of Ascaris megalocepltala . . 452

355. Stage in the development of a "ball-egg" of Ascaris megalocephala cor-

responding to the 8-cell stage in the development of a normal egg . 453

356. Stages in the early development of Asterias vulgaris . 462

357. Young larvae of Asterias vulgaris ... . 463

358. Fully developed Bipinnaria larva of Asterias vulgaris, about three weeks old 465

359. Larva of Asterias vulgaris, four days old, viewed from the dorsal surface,

showing two madreporic pores . . . . .466

ILLUSTRATIONS xxix

360. Lateral views of an advanced Bipinnaria of Axt< r/«/s rii/i/nris in which the

brachiolarian arms are just appearing ... . 468

361. Ventral view of a Bipinnaria of Asterias rult/ta-is, of the same age as that

shown in Fig. 360, in order to show the mutual relations of the coelomie
cavities ......... 469

362. Lateral views of the brachiolarian phase of the larva of Asterina rn/i/itris

in various stages of fixation and metamorphosis .... 470

363. Frontal longitudinal sections of two early embryos of Asterinn gibbosn in

order to show the development of the, coelom .... 473

364. Views of a free-swimming larva of As/cri/ia gibbosa, five or six days old . 474

365. Longitudinal frontal sections of larvae of Asterina gibbosa in order to

show the segmentation of the coelom and the origin of the hydrocoele

and madreporic vesicles ....... 475

366. Longitudinal frontal sections of larvae of Asterina gibbosa, seven to eight

days old, in order to show the beginning of the metamorphosis . . 476

367. Views from the side of a larva of Asterina gibbosa, seven days old, in the

initial stages of metamorphosis ...... 477

368. Views from the side of a larva of Asterina gibbosa, eight days old, showing

further progress in the process of metamorphosis .... 478

369. Longitudinal frontal section through a larva of Asterina gibbosa about the

same age as those shown in previous figure .... 478

370. Dorsal (i.e. aboral) views of two young specimens of Asterina gibbosa

shortly after the metamorphosis ...... 479

371. Three figures illustrating the development of the genital stolon, genital

rachis, and gonad in Asterina gibbosa ..... 480

372. Longitudinal frontal section of the larva of Solastcr endeca . . . 482

373. Early stages in the development of Ophiothri,'- fragifis . . . 485

374. Longitudinal frontal sections of early larvae of Ophiothrix fragilis . 486

375. Ventral views of young larvae of Ophiothrix fragilis . . . 488

376. Ventral view of fully developed larva of Ophiothrix fragilis, sixteen

days old .... .... 489

377. Three diagrams illustrating the internal changes which occur in the larvae

of Ophiothrix frayilis up to the end of the first period of metamorphosis . 493

378. Longitudinal frontal section of a larva of Ophiothrix frayilis in the first

stage of metamorphosis . . 494

379. Two larvae of Ophiothrix fragilis in the concluding stages of metamor-

phosis, viewed from the ventral side ..... 496

380. Transverse sections through the discs of two young brittle-stars in order to

show the origin of the germ cells ... . . 4'.i7

381. Two diagrams designed to elucidate the mutual relationships of stone-

canal, dorsal organ, axial sinus, madreporic vesicle, genital rachis, etc.,

in an Asteroid and an Ophiuroid respectively .... 500

382. Ventral view of the larva of o/i/iiurn brcvis during the metamorphosis . 502

383. Two stages in the segmentation of the egg of Strongyloeentrotus lividus.

(The segmentation of the egg of Echinus esculcntus pursues an identical
course) .... . 507

384. Early stages in the development of Echinus esculent us . . 508

385. Young larvae of Echinus esciihntits, viewed from the dorsal surface . 509

386. Echinopluteus larva of Echinus esculcntus, about eleven days old, viewed

from the dorsal surface, in order to show the formation of the ciliated
epaulettes ... .510

387. Echinopluteus larva of Echmus esculentus, twenty-three days old, viewed

from the dorsal surface . . . • • .512

xxx INVEETEBKATA

FIG. ''A015

388. Diagrammatic; transverse sections through the "Echinus-rudiment" of

Echinoplutei larvae of Echinus esculent us, ranging in age from twenty-one

to fifty days ....... .513

389. Diagrammatic side-views of the larvae of an Asteroid, Echinoid, and

Balanoglossid in order to show the comparability of the apical plate of

an Asteroid with the larval brain of the other two types of larvae . 516

390. Echinopluteus larva of Echinus esculcntus, about fifty days old, just about

to metamorphose, viewed from the left side .... 517

391. Oral and aboral views of young sea-urchins immediately after the meta-

morphosis . • 519

392. A series of diagrams showing the changes which the gut undergoes in

Echinus esculentus after metamorphosis. The diagrams represent hori-
zontal sections through the young imago . . . 521

393. Types of Lithium larva . . 527

394. The 32-cell stage in the segmentation of the egg of Synapta digitata,

viewed from the side ..... . 531

395. The free-swimming gastrula of Synapta digitata .... 531

396. Two young larvae of Synapta digitata, viewed from the side . . 532

397. Three views of young Auricularia larvae of Synapta digitata, viewed from

the dorsal surface, showing the division of the coelom . . . 534

398. The fully-developed Auricularia larva of Synapta digitata, viewed from

the ventral surface and from the side ..... 535

399. Diagrams of the anterior aspect of metamorphosing larvaeof Synapta digitata

in order to show the changes undergone by the longitudinal ciliated band 537

400. Metamorphosing larva of Synapta digitata, viewed from the ventral aspect 538

401. Pupa of Synapta digitata in two stages of development . . 540

402. Post-larval stage in the development of Cucumaria saxicola, viewed from

the side . 543

403. Early stages in the embryonic development of Antedon rosacea . . 546

404. External views of the embryo and larva of Antedon rosacea showing the

mutual relations of stomodaeum and ciliated bands . . . 548

405- External views of larvae of Antedon rosacea at the time of hatching and

after fixation in order to show the development of the calcareous ossicles 549

406. Longitudinal sections through free-swimming larvae of Antedon rosacea . 550

407. Fixed larva of Antedon rosacea, three and a half days after hatching,

viewed from left side (decalcified) . .551

408. Fixed larva of Antedon rosacea in which the vestibule is open but in which

no trace of the arms have as yet appeared ..... 553

409. Calyx of a larva of about the same age as that represented in Fig. 408,

decalcified and cleared in order to show the internal structures . . 554

410. Fixed larva of Antedon rosacea, viewed from the side, in order to show the

origin of the arms . . • 555

411. View of the calyx of a fixed larva of Antedon rosacea from the upper side

in order to show the adhesion of the lobe of the hydrocoele to the arm

and the first dichotomy of the arm . 556

412. Map showing the mutual relations of the ossicles in the base of the calyx

of a fixed larva of Antedon rosacea Avhen the adult condition has been
nearly attained . • 557

413. The stalked larva and adult form of Antedon multispina . . 559

414. Diagrammatic reconstruction of the common ancestor of the phylum

Echinodermata, and diagrams showing the modifications which the
descendants of this ancestor underwent in becoming the ancestors of the
Eleutherozoon and Pelmatozoon stocks ..... 563

ILLUSTKATIONS xxxi

K1O. 1'AilK

415. Early stages in the development of Balanoylossu-s claviycriis . 571

416. Later stages in the development of Balanoglossus clai-tijcrus . . 572

417. Still later stages in the development of £alan<><//<>sxt<:-< cltn-iiji-riix . . 573

418. Surface view of the young Tornaria larva of Balanoglossus flitr!tj<irus, four

days old ......... 574

419. Illustrating the structure of the apical plate and eyes of a full-grown New

England Tornaria larva ....... 575

420. Illustrating the origin of the middle and posterior coelomic vesicles in the

New England Tornaria . . . . . . .576

421. Full-grown New England Tornaria, seen from the left side . . 577

422. Illustrating the metamorphosis of the Bahamas Tornaria . . . 578

423. Illustrating the development of the dorsal nervous system in the meta-

morphosing Bahamas Tornaria ... ... 579

424. Sagittal section through the New England Tornaria immediately after

the metamorphosis into the Balanoglossid worm .... 580

425. Portions of transverse sections through the trunk region of three young

Balanoglossid worms of different ages in order to illustrate the develop-
ment of the genital organs in the Bahamas species . . . 581

426. The larva of Dolichoylossus pusillus in the act of escaping from the egg-

membrane ......... 583

427. Longitudinal frontal sections through two embryos of Dolichoglossus

pusillus in order to illustrate the development of the body-cavities . 584

428. Stages in the segmentation of the egg of Amphioxus lanccolatus . . 588

429. Stages in the gastrulation of the egg of Amphioxus lanccolatus. All the

figures represent sagittal sections ...... 500

430. Diagrams showing the parts played by ectoderm and endoderm in the

process of gastrulation in A mphioxus lanccolatus .... 592

431. Transverse sections through an embryo of Amphioxus lanceolatus just

after the completion of gastrulation in order to illustrate the develop-
ment of nerve-cord, notochord, and coelom .... 593

432. Transverse sections through an older embryo of Amphioxus lanccolatus

than that represented in the previous figure to show the further develop-
ment of nerve-cord, notochord, and coelom .... 594

433. Illustrating the formation and development of the head-cavities of

Amphioxus lanceolatus ....... 595

434. Diagram of longitudinal section of Amphioxus lanccolatus parallel to the

sagittal plane but lying to one side of the middle line in order to show

the mutual relationships of head, collar, and trunk-cavities . . 596

435. Illustrating the mutual relationships of collar-cavities and splauchnocoeles

in Amphioxus lanccolatus ... ... 597

436. Two young larvae of Amphioxus lanccolatus, seen from the left side . 598

437. Larva of Amphioxus lanccolatus with four primary gill-slits, seen from the

left side ......... 599

438. Diagrammatic transverse sections through the hinder region of two young

specimens of Amphioxus lanccolatus in order to show the origin of
sclerotomes . . . . . . . . . « 600

439. Illustrating the development of the excretory organs of Aiivpliioxus

lanccolatus ......... 601

440. Illustrating the development of the genital organs of Amphioxus lanccolatus 602

441. Illustrating the metamorphosis of the larva of Amphioxus lanccolatus . 603

442. The egg of Cynthia partita before and during fertilization . . 610

443. Stages in the segmentation of the egg of Cynthia partita . . 612

444. Illustrating the gastrulation of the egg of Cynthia, partita . . 615

xxxii INVEKTEBKATA

FIG. I'Ar.K

445. Sections through eggs of Cynthia partita in order to illustrate the changes

in form undergone by ectodermal and endodermal cells during the pro-
cess of gastrulation . ....... 616

446. Illustrating the closure of the blastopore in the gastrula of Cynthia partita 617

447. Optical sagittal section of gastrula of Cynthia partita . . . 618

448. Dorsal view of an embryo of Cynthia partita after the closure of the

blastopore in order to show the formation of the tail . . . 618

449. Transverse section through the middle of a gastrula of Cynthia partita . 619

450. Longitudinal sagittal section of tadpole of Cynthia partita just before it

escapes from the egg-membrane ...... 620

451. Free-swimming tadpole of the simple Ascidian Ciona intestinalis, seen from

the side ......... 621

452. Anterior portion of free-swimming tadpole of the simple Ascidian Phallusia

mammilata, seen from above ...... 621

453. Illustrating the metamorphosis of the tadpole of Ciona intestinalis . 623

454. Transverse sections through the brains of Ascidian tadpoles in order to

illustrate the development of the hypophysial tube and of the adult
ganglion ......... 624

455. Longitudinal sagittal sections through the brain vesicles and hypophysial

tubes of just fixed tadpoles of Ciona intestinalis .... 625

456. Transverse sections through the hinder part of the pharynx of a series of

larvae and just fixed young of the simple Ascidian Ciona intestinalis
in order to illustrate the development of the heart pericardium and
epicardium ......... 627

457. Illustrating the development of the genital organs in the simple Ascidian

Molcjula ampulloidcs ....... 629

458. Illustrating the result of the development of single blastomeres of the

2-cell stage of the egg of Cynthia partita ..... 631

459. Section through the segmenting egg of Pyrosoma yigantcum at the stage

of thirty-six blastomeres ....... 633

460. Longitudinal sections through two embryos of Pyrosoma giyanteum in

order to show the formation of organs in the Cyathozooid . . 633

461. Two embryos of Pyrosoma giganteum, viewed from the doi'sal surface, in

order to show the formation of organs in the Cyathozooid . . 634

462. The embryo of Salpa fusiformis attached to the maternal placenta, seen

from the side ........ 636

463. Budding stolon of Pcrophora listen showing the development of buds from

the septum of the stolon ....... 638

464. Stages in the development of the bud of Distaplia maynilarva . . 639

465. Lateral view of old bud of Distaplia maynilarva .... 640

466. Primordial colony of Pijrosoma giyantcum consisting of four Ascidiozooids

coiled round the degenerating Cyathozooid .... 641

467. Bud of a Botryllid almost completely developed and bearing two young

buds, seen from the dorsal side ...... 642

468. Four stages in the budding of a Diplosomid Ascidian . . . 643

CHAPTER I
INTKODUCTION

THE science of Embryology has for its subject-matter the growth of
animals from the time when they first appear as germs in the bodies
of their parents until they reach the adult condition, and are
able to produce similar germs themselves. It thus includes a study
of the complete life-cycle, and is much more extensive in its scope
than ordinary descriptive Comparative Anatomy which confines itself
to a study of the adult forms.

In practice, however, the study of the adult form precedes the
study of all other stages of the life-history, because it is assumed that
in the adult producing ripe germs, we have a stage which is the same
whatever kind of animal we examine. A text-book of Embryology
therefore assumes a knowledge of the adult forms of the animals
whose life-histories it describes. Even with this limitation the scope
of Embryology would be enormous were it not for a defect which is
often overlooked, but which renders it possible to bring the most
important results before the reader within moderate compass ;
this defect is the extreme difficulty of finding out with any com-
pleteness the whole course of any given life-history.

The life-history of an animal is only in the rarest cases directly
observed ; it is deduced from a comparison with one another of in-
dividuals of various ages, and only when we can examine a large number
of individuals belonging to stages separated from one another by very
short intervals can we get any reliable results. Numberless mistakes
have been made in the past and will continue to be made in the
future, by the effort to re-construct a life-history from the observation
of an insufficient number of stages. Thus, to give examples, the
germ cells of Balanoglossus and of the Annelid Lopadorliynchus have
been stated to arise from the ectoderm, whereas in reality in both cases
they arise from the lining of the body -cavity or coelom. Sometimes the
life-history has been actually read backwards : thus the later stages in
the Toruaria larva have been regarded as the earlier. In the case of
the vast majority of animals only bits and scraps of the life-history
are known, and the number of cases in which the whole course of
VOL. i B

2 INVERTEBEATA CHAP.

this history is thoroughly known are very few. Hence a careful study
of these few cases must suffice to include the certain and indisput-
able results of the science of embryology. Outside this limited field
are a number of suggestive facts from which no certain conclusions
can be drawn, but which serve as clues to indicate those lines
for future research which will probably give the most interesting
results ; some of these will be referred to in the following pages.

The germs from which animals spring are of two kinds — (a) those
that can develop directly, or asexual germs ; and (6) those that under
ordinary circumstances are incapable of development until they have
united or "conjugated" with another germ. These latter are the
sexual germs, and in all the animals which we shall have to consider
they are unicellular, and are of two kinds, viz. comparatively large non-
motile germs or ova (eggs), and small motile germs or spermatozoa.
The organism which produces the ova is termed the female, that
producing the spermatozoa, the male, and that which results from the
union or conjugation of these two types of germ is called a zygote.
If, as often happens, both kinds of germs are produced by the same
adult, this is termed a hermaphrodite. In this case, however, the
spermatozoa usually ripen before the ova and the animal is said
to be protandrous. A case where the eggs ripen before the male
germs is very rare amongst animals, but is commoner amongst
flowering plants, such an organism being termed protogynous.

Most asexual germs are multicellular, containing several nuclei
and in some cases portions of more than one tissue of the parent.
Such germs are called buds, a.nd the laws of bud development are as
yet most imperfectly known, but in many cases they seem to differ
markedly from those governing the development of the zygote. In
this book our attention will be directed mainly to the development
of the zygote, but the most important facts about bud development
will also be given. Some asexual germs are called parthenogenetic
ova, because in development and appearance they resemble true ova,
from which they differ only in being able to undergo complete
development without conjugating with spermatozoa. The develop-
ment in this case is the, same as that exhibited by true ova.

The development of ova and of spermatozoa, from their first
appearance until they become capable of union with one another, is
known as gametogenesis, since gamete is a convenient word to
designate both kinds of sexual germ. It is called oogenesis for the
ova and spermatogenesis in the case of spermatozoa.

Both forms of germ when first distinguishable are small, rapidly
dividing cells which are often termed primitive germ cells. In
these divisions the nuclear substance, which absorbs stain — the
chromatin — becomes arranged in the form of a definite number
of rods or chromosomes — denoted by the symbol 2x. The actual
number is characteristic of the species in question, and it is often
assumed, and is taught in most text-books, that this number is
characteristic of the nuclei of all the cells in the body when they

i INTRODUCTION 3

proceed to division. But this is by no means universally the case ;
in fact in several cases which have been subjected to detailed examina-
tion it has been proved not to be the case.

The germ cells in this state of rapid division are termed oogonia
and spermatogonia respectively. Division is succeeded in both
cases by growth and then by a state of rest, at the end of which the
germs are known respectively as oocytes and spermatocytes of
the first order. In most cases during this period the difference
between the two kinds of germ becomes apparent. The spermatocytes
increase only slightly in size as compared with the spermatogonia
and undergo no diminution in number ; but some only of the oogonia
increase in size and become the large oocytes or unripe ova ; the
remaining oogonia are either absorbed as food by their successful
sisters, or reduced in size so as to form " follicle cells " which serve
as a protective covering for the oocytes.

The follicle cells in many if not all cases contribute nourishment
to the oocyte, and a considerable portion of this food, termed
deuteroplasm or food-yolk, is precipitated in the form of globules or
platelets consisting chiefly of lecithin. A first stage in the storing
of food material in the cytoplasm appears to be the emission into the
cytoplasm of chromatin from the nucleus. This process has been
studied in detail in Echinoderm eggs by Schaxel (1911). Yolk
globules appear later, at first near the periphery of the egg, by the
transformation of this cytoplasinic chromatin. Often indeed the
modified cytoplasm infiltrated with chromatin is aggregated in a
more or less spherical body which absorbs stain, termed the yolk-
nucleus (Fig. 11, y.ri}; round this the yolk first appears, but after
the completion of yolk formation it disappears. Occasionally, as
Schaxel has shown to be the case in the egg of Strongylocentrotus, no
yolk at all is formed, the deposits of cytoplasinic chromatin con-
stituting the only reserve material present. Different eggs differ from
one another in the amount and nature of the food-yolk. The follicle
cells in many cases have as their final duty the secretion of an
outer egg-shell or chorion (Fig. 11, cli). The inner egg-shell is
secreted after fertilization by the cytoplasm of the egg itself and is
termed the vitelline membrane.

The nucleus of the unripe ovum is in nearly every case
distinguished by the fact that it has the form of a vesicle con-
taining a clear fluid termed the nuclear sap, within which is a
dense mass of staining matter, different in chemical reactions from
chromatin, which is termed the nucleolus. Stretched across the
nuclear sap are a few fibres and on these the true chromatin is
situated as small inconspicuous grains. This arrangement of material
gives the nucleus of the oocyte a peculiar look which is unmistak-
able and which led to its being termed the germinal vesicle by the
older writers, whilst the nucleolus was termed the germinal spot.

Before male and female germ cells can unite both must mature,
and this they do by undergoing two maturation divisions. The

4 INVERTEBEATA CHAP, i

changes which the nucleus undergoes previous to, and during, these
maturation divisions, have been studied with great minuteness
by a large number of observers, and on many important points a
general agreement has been arrived at. An excellent summary of
the present stage of our knowledge has been given by Agar (1911),
who has worked out the development of the male cells in the Dipnoau
fish Lepidosiren.

As maturation approaches, the chromatin granules in the nuclei
of the spermatocytes of this species become aggregated into long
ribbons, which are the chromosomes. This stage is termed leptonema,
and the chromosomes in this stage are termed leptotene threads ; they
appear in double the number that are found in the ripe ovum when
ready to receive the spermatozoon. This double number is known as
2 x. There is a large conspicuous nucleolus present as in the unripe
egg (Fig. 1, A, ?i). The leptotene threads continue to shorten and
become thicker and thus they pass into the stage of zygonema, in
which the threads become opposed to one another in pairs and are
termed zygotene threads (Fig. 1, B). Then the members of each
pair fuse with one another. Thus the stage of pachynema is attained
in which there are only x shorter thicker pachytene threads or chro-
mosomes, arranged in the form of U's in a "bouquet" at one side of
the nucleus.

Here we arrive at a fundamental divergence of opinion between
two groups of workers. The changes which we describe cannot, of
course, be observed in the living nucleus, but must be inferred from
the comparison with one another of fixed and stained nuclei. Some
workers maintain that nuclei with x pachytene threads represent the
first stage in maturation, and that the stage with 2 x zygotene threads
represents an attempt at longitudinal division of these chromosomes,
which is, however, abortive. Agar, however, points out that in the
material which he studied the leptotene threads cross each other at
all angles, and when the process of amalgamation in pairs or syndesis
begins, at first only one end of each member of a pair of zygotene
threads is parallel with its fellow, the other end passes into an
irregular tangle. He, therefore, in common with a great number of
workers, interprets the appearances seen in the beginning of the
pachytene stage as the beginning of a side -by -side fusion of
originally separate chromosomes — i.e. as parasyndesis. This stage
is followed by one in which the two elements forming the pachytene
chromosome separate in the middle, and the chromosome is trans-
formed into an elongated ring which is twisted on itself (Fig. 1, C).
This is the stage of strepsinema, the rings being termed strepsitene
threads. The two sides of each ring separate from one another, first
at one end, so that the ring is converted into an elongated V, and
then at the other so that the two original constituents of the ring
are again entirely separated from one another and the original
number of chromosomes, 2 x, is restored.

During the strepsinema stage a process called synizesis begins.

FIG. 1. — Eight views of the maturation of the male cells of
Lepidosi re n jiitraifii.i-i/. (After Agar.)

A, leptonema stage. B, beginning of zygonema. C, strepsinema stage, beginning of syni/esis.
D, separation of two chromosomes wliich were united in syndesis completed ; nuclear membrane dis-
appeared. E, second pairing of chromosomes begun, appearance of centrosomes for the first matura-
tion spindle. F, later stage in second pairing of chromosomes, the centrosomes of the first spindle
now situated at opposite poles of the nucleus. G, the anaphase of the first maturation division. 11,
the metaphase of the second maturation division. &i, a chromosome which has not yet paired with its
fellow ; U2, two chromosomes united end to end ; b3, two chromosomes united in a ring ; c, centrosome
of spindle of first maturation division ; I (in D), the two longest chromosomes, (in K), the t\\" lon^.'si
chromosomes united end to end, (in G), the two longest chromosomes scpanitii]-; from i-ai-h other iii
the first maturation division, (in II), one of the longest chromosomes dividing into two in the second
maturation division ; H, nucleolus.

6 INVEKTEBKATA CHAP.

This is the aggregation of the chromosomes iu a kind of hunch at
one side of the nucleus. This persists for a time, hut eventually
the chromosomes separate out again from one another, a process
known as diakinesis. The rings of the strepsitene stage are com-
pletely hroken up into their constituent parts, and the number 2 x
is consequently restored by the time that diakinesis has reached its
utmost limit.

During diakinesis the chromosomes become driven apart from
one another and become spread out under the nuclear membrane,
and the uucleolus during the same time gradually loses its staining
power and disappears from view. The nuclear membrane then
disappears and the nuclear sap mingles with the cytoplasm (Fig. 1, D).
At the same time, the centrosome, which forms the centre of the polar
rays in every nucleus undergoing karyokinesis, and which lies at the
side of the resting nucleus, is seen to have divided into two daughter
centrosomes (Fig. 1, E c) ; they are already moving apart to take up
positions at opposite poles of the nucleus, whilst between them the
rays of the achromatic spindle are already developing.

The chromosomes, which become much shorter and thicker,
now join end to end in pairs ; but their free ends then swing round
and join one another, so that eventually parasyndesis again occurs
(Fig. 1, F &1, 62, and &3), and the number of chromosomes is again halved,
and we thus obtain x short, thick, ring-like chromosomes which
become arranged in a plane so as to form the equatorial plate of the
first spindle.

The division of the nucleus then takes place ; each daughter
nucleus receives one half of each ring, and these halves represent the
separate chromosomes of the diakinetic stage which subsequently fused
with another (Fig. 1, G).

In the case of the testis the division of the nucleus is followed by
the division of the germ cell into two equal cells, and in this way two
spermatocytes of the second order are formed : the undivided germ
cell with its nucleus and condensed chromosomes being termed the
spermatocyte of the first order. The nuclei of the spermatocytes
of the first order do not undergo a resting stage, but in each of
them a new spindle is formed at right angles to the first, and each
chromosome becomes split longitudinally so that at the eu suing
division of the nucleus one half of each chromosome goes into each
daughter nucleus (Fig. 1, H).

If this description has been followed it will be seen that, in the
first maturation division whole chromosomes go to each daughter
nucleus — this is termed the reducing division ; whilst in the second
division one half of each chromosome goes to each daughter nucleus
— this is termed the equating division.

The division of the nucleus is again followed by the division of
the cell, and in this way four cells are derived from each spermato-
cyte of the first order. These cells are termed spermatids and each
spermatid becomes converted into a spermatozoon. The manner in

i INTRODUCTION 7

which this change is effected seems to be fundamentally the same in
most animals which have been examined. One of the best and most
recent accounts of it is that given by Duesberg (1909), who worked
on the development of the spermatozoa of the rat. According to this
author the spermatid is a small polygonal cell containing a large
resting nucleus, at one side of which is the centrosome which
functioned in the last maturation division. This centrosome has
already divided into two minute centrioles lying one above
the other (Fig. 2, A, c1, c). Besides the centrioles there is a
peculiar body embedded in the cytoplasm termed the idiosome,
apparently derived from the sphere or modified cytoplasm which sur-
rounded the ceutrosome, although it is now widely separated from the
centrioles. The distal or outer centriole begins to give rise to a thin
filamentous fiagellum which is the rudiment of the tail of the
spermatozoon, whilst the idiosome travels to the opposite side of the
nucleus from that on which the centrioles lie, and becomes applied
to the nuclear membrane and forms a cap-like structure known
as the acrosome. The nucleus sends out a prolongation which
reaches the lower or proximal centriole, and this becomes applied to
the nuclear membrane and forms a plate-like thickening on it. The
nucleus carrying the acrosome then begins to emerge from the
cytoplasm on the opposite side of the cell to that on which the
ceutrioles are situated. Both centrioles are dragged after the
nucleus. Round the upper or immersed half of the nucleus the
cytoplasm is differentiated so as to form a funnel of clear substance
called the " ruffle " (manchette) (Fig. 2, D, m). The nuclear sap is
then apparently expelled and the nucleus converted into an almost
uniform mass of staining matter. Its form changes — no longer
spherical, it becomes sickle-shaped (Fig. 2, E). The distal centriole
divides into two daughter centrioles, and to the lower and proximal
of these, the tail filament, now greatly grown in length, is attached,
whilst the upper or distal one forms a ring surrounding the filament.
The nucleus now emerges completely from the cytoplasm. It forms
the head of the spermatozoon ; the ruffle disappears, but the acre-
some is still distinguishable as a thickening on the convex side of
the sickle. The cytoplasm now forms a thick mantle surrounding
the lower part of the filament (Fig. 2, G). The ring-shaped centriole
travels away from the nucleus along the filament till it reaches
a definite position. The cytoplasm shrinks more and more and is
eventually completely cast off. The ring-shaped centriole and the
piece of the filament between it and the nucleus forms the middle-
piece of the spermatozoon. When these changes are complete the
spermatid is transformed into a spermatozoon, begins to exhibit
active movement, and is capable of fertilizing a ripe egg.

We must now turn our attention to the process of maturation of
the egg. We left the egg in the stage when the nucleus was
inordinately swollen with cell sap, and when there was a large
nucleolus. All the changes exhibited by the ripening sperinatocyte

D

FIG. 2. — Nine stages in the transformation of a spermatic! into a spermatozoon.

(After Duesberg. )

A, spermatid with two centrioles, the proximal and the distal, at one side of nucleus and the idio-
some at the other side. B, stage in which the distal centriole is giving rise to a filament, and in
which the idiosome is applied to one side of the nucleus. C, stage in which the nucleus is beginning
to emerge from the cytoplasm dragging after it the centrioles; the filament, now grown longer, is im-
mersed in the cytoplasm, the ruffle has appeared, and the idiosome has become the acrosome. D, stage
in which the nucleus has begun to bocome sickle-shaped. E, stage in which the distal centriole has
divided into two and the outer one has become a ring. F, stage in which the ring is moving outwards
along the lilament. G, stage in which the ring has moved beyond the cytoplasm. H, I, two stages in
casting off the cytoplasm, etc, Acrosome ; c, proximal centriole ; ci, distal centriole ; M, idiosome ; m,
ruffle (manchette) ; r, ring centriole.

8

CHAP, i INTRODUCTION 9

are exhibited also by the oocyte of the first order, as wo term the egg
when it has reached its full size. Its nucleus passes through the
stages of leptouema, zygonema, pachynema, strepsiueina, etc. The
nucleolus disappears, the nuclear membrane dissolves, and the nuclear
sap mingles with the cytoplasm. The cousefjiience of this is, that
since the chromosomes form a small and inconspicuous mass, the egg,
viewed under the low power of the microscope, appears to have lost
its nucleus, and this is a ready way to distinguish unripe from ripe
eggs, or in other words, oogonia from oocytes of the first order.

The great difference between oocytes and spermatocytes of the
first order is that in the case of the latter when the cell divides, it
gives rise to two daughter cells of the same size which form
spermatocytes of the second order, but when the oocyte divides, it
forms two daughters of unequal size, the larger forming the oocyte
of the second order whilst the smaller forms a rudimentary cell
incapable of development, termed the first polar body. At the
second maturation division the same phenomenon repeats itself, the
oocyte of the second order divides into two unequal daughters — the
larger is the ripe ovum, whilst the second is again a rudimentary
cell which never develops and which is termed the second polar
body. The first polar body often divides into two daughters of
equal size which are, like the second polar body, to be regarded as
sisters of the egg, or better, as rudimentary eggs (Figs. 3, B, and 4, B).
The same sacrifice of quantity to quality therefore which is seen in
the absorption of many oogonia by their more fortunate sisters, repeats
itself in the maturation divisions.

The ripe egg can now receive the spermatozoon. As soon as the
head of the first spermatozoon has penetrated the egg an alteration of
the surface of the latter usually takes place, which cuts off the tail of the
spermatozoon and prevents any other spermatozoa from, entering;
the middle piece of the successful spermatozoon, however, follows the
head into the egg. This alteration in the surface of the egg has
been diagnosed by Loeb as a kind of cytolysis : for it can be observed
that a number of fine globules issue from the surface of the egg, and
that their outer surfaces coalesce to form the inner egg-shell or vitelline
membrane.

Meanwhile the spermatozoon head within the ovum swells up, it
assumes a vesicular form, and nuclear membrane, cell sap and
chromosomes can be again demonstrated in it. The middle piece
takes on the character of a centrosorne and around it the achromatic
ra'ys appear, forming what is termed an "aster." The male pro-
nucleus, as the spermatozoon head is now termed, moves towards the
residual nucleus of the egg, termed the female pronucleus, which in
its turn advances towards the male. Male and female pronuclei
then meet and fuse and form a single nucleus, the zygote nucleus,
and fertilization is complete.

After a resting period of an hour or two the zygote nucleus
begins to prepare for karyokinesis, and the spindle is so formed that

10

INVEETEBEATA

CHAP.

its equatorial plate lies at right angles to both female and male pro-
nuclei, and so both are halved at the ensuing division and equal
parts of both distributed to the first two cells into which the ovum

B

.OQ

nMt

",--?i

• V- - / . / \ I ;\J~
f

- o • - .--

-,'•?•— •r'Sf). •/'"S ' >i>i ^'--'T" 'A<t '"'':• ' '"rt'P(x^-' '.-.'•. '• ,.' ' \ .'/•^i^'.'"^'-^

«• i- m $$ «^

^~i>yy-i .r. . : »rQM^I foO.,^-M

I >«X .- . : > ^ ""^T^^"

Q^^l

FIG. 3. — Four stages in the maturatiou and fertilization of the egg of Orepidula jil.ii.ini.

(After Conklin.)

A, formation of first polar body ; the spermatozoon lias entered the egg and has begun to swell up
into the male yronucleus. B, formation of second polar body ; the first polar body has divided into
two. C, the male and female pronnclei have come together. D, formation of the first cleavage spindle ;
the female prouucleus above and the male pronucleus below are still clearly distinguishable from one
another. fi>, Female pronucleus ; mji, male pronucleus ; y>' (in A), iir^t polar body, (in B and C), two
cells resulting from division of first polar body ; p2, second polar body.

divides. In some few cases it is possible to distinguish in this first
equatorial plate the chromosomes derived from male and female
pronuclei respectively, for they are of different sizes and arranged
in two different groups. This is especially clear in the egg of Crepi-

INTRODUCTION

11

dula planet, a species iu which the processes of maturation and
fertilization have been worked out in great detail by Couklin
(1902). The ceutrosomes of the first cleavage spindle are here
stated to be derived from the division of the sperm centrosome. It
is therefore reasonably
certain that in all cases
each daughter cell re-
ceives a half of each male
and female chromosome.

It is by no means
always true that the
spermatozoon can only
enter the egg after the
formation of both polar
bodies. In many cases
it enters the egg whilst
it is still an oocyte of
the first order, and even
before the nuclear mem-
brane has been dissolved
and the germinal spot
has disappeared. This is
true of the eggs of many
Annelida and Mollusca.
In other cases, such as
in some Ascidians, the
first maturation spindle
is formed before the
spermatozoon enters, but
the first maturation
division is not completed
till the spermatozoon is
inside the egg. Finally,
in Dinophilus according
to Shearer (1912), the
spermatozoon enters the
oogonium and remains
passive during the growth

FIG. 4. — Two stages in the first division of the fertilized
egg of Crepidula plana. (After Conklin.)

A, the first cleavage spindle ; female chromosomes above
separated by an interval from male chromosome below. B, the

and maturation of the
germ cell.

If the eggS are Stale, division of the zygote nucleus is complete. /, Female cliromo
i 6 if tlieV have been somes> "'."'^le chromosomes; 2i!(in A), lirst polar body, (in B),

products of division of lirst polar body ; jft, second polar body.

shed too long irom the

ovary before being fertilized, then more than one spermatozoon can
enter them, and an extra centrosome is thus introduced, between
which and one or both of the centrosomes resulting from the division
of the centrosome of that sperm which has actually effected fertiliza-
tion, extra achromatic fibres can be developed and irregular division

12

INVEETEBEATA

CHAP.

of the egg results ; in most cases this takes the form of simultaneous
division into four equal parts.

In the case of large eggs, like those of birds, it appears that
normally a considerable number of spermatozoa enter the egg. One
only unites with the female pronucleus and forms the zygote nucleus,
the rest divide independently and form groups of small cells which
are produced by the aggregation of the cytoplasm round the products
of their division. Soon, however, the cells formed round the
daughters of the zygote nucleus crush out and kill these other cells,
and the former alone enter into the formation of the embryo.

It appears therefore that the alteration of the surface of the egg
so as to exclude supernumerary spermatozoa, which is so marked
a feature in small eggs, must be due to some chemical influence
radiating from the zygote nucleus, and that in large yolky eggs it
does not reach sufficiently far to prevent the entry of extra
spermatozoa at some distance from the first one.

The sequence of events worked out by Agar for the maturation of
the nuclei in the male cells of Lepidosiren agrees fairly closely with
that described by other workers for other forms. But in many cases,
before the first maturation division has taken place, when in the
paired or bivalent chromosomes the components are beginning again
to separate, a longitudinal split appears at right angles to the split
separating the components ; this is the anticipation of the final
division of each chromosome into longitudinal halves which occurs in
the second maturation division. We thus get quadripartite chromo-
somes, which are termed tetrads. Further, many workers maintain

that in the final pairing of chromosomes
which takes place just before the first
maturation division, there may in some
species be an end -to -end junction,
metasyndesis, instead of a side-to-side
junction or parasyndesis.

When a substance like chromatin
appears in the ripening eggs and
spermatozoa, in exactly the same
forms, generation after generation, and
when the masses of chromatin con-
tinually undergo complicated changes
of shape in the same order, it is
natural to imagine that such a sub-
stance must be of great importance in
the main function of the germ cells, i.e.
transmitting the hereditary qualities of
the parents ; as a matter of fact it was on the casting off of the
two polar bodies as a preliminary to development, and on the nuclear
changes which accompany this phenomena, that Weismann (1886)
founded his famous theory of heredity. According to him the nucleus
of the egg was supposed to have a portion of its material charged

FIG. 5. — Polar view of the first
maturation division of the male
germ cells of Alyihis 2)ilwiil-i<s,
in order to show tetrads.
(After Wilson. )

i INTKODUCTION 13

with the function of producing the peculiarities of the cytoplasm
of the unripe egg — the amount, colour, and composition of the food-
yolk, etc. When this task was accomplished and the ovum was ripe,
it was supposed that this portion of the nucleus, termed by Weis-
maim histogenetic plasm, was extruded as the first polar body.
The extrusion of the second polar body he explained by his theory
of "ids."

According to this theory, the material basis of the transmission of
the parental qualities to the child is contained in the chromatiu
which is organized into a number of " ids." Eacli " id " contains
within itself the whole potentiality of the animal, i.e. one " id " alone
is capable of causing the egg to develop into an adult animal. The
" ids " are similar, but not exactly the same, and the animal which
develops is a compromise between the potencies of the various "ids."
The " ids " are capable of assimilation and growth, and in each
longitudinal division of the chromosome each " id " contained therein
is divided into two precisely similar daughter "ids," but in the
transverse or reducing division (which in Weismann's day was
supposed to be the second, not the first division) different " ids " are
separated from one another.

This is what happens in the formation of the second polar body,
and now the spermatozoon brings in an equal number of " ids " and
thus the number originally present in the oogonia is restored. Since
the " ids " of the spermatozoon are not exactly the same as those of
the egg, and since Weismann assumed that the casting forth of half
the maternal "ids" might take place at random, i.e. might consist of
any group of the "ids " amounting to half the number, the basis was
given for inheritable variations, because different combinations of
maternal and paternal " ids " might come about by a difference in
the " ids " which were cast forth at the reducing division.

It is one great merit of Weismann's theories that, whatever may
be thought of their truth or untruth, they have acted as powerful
stimulants to research. Hertwig (1890) published a work on the
spermatogenesis and oogenesis of the worm, Ascaris megalocephala,
in which he showed, for the first time, the parallelism in the changes
which occur during the ripening of both kinds of germ cell, and
proved that the polar bodies were the degenerate sisters of the egg,
thereby overthrowing Weismann's theory of the histogenetic plasm.
But Weismann's theory of the meaning of the reducing division
was not thus disproved, although of course it was shown that it was
the first, not the second maturation division in which whole chromo-
somes were separated from one another, and to which Weismann's
hypotheses must apply. This theory was shattered by the work
which ensued on the discovery of what have been called sex-
chromosomes, by McClung, Wilson, and other American workers.
Wilson has given an excellent summary of the whole subject (1911),
and to this we must now address ourselves.

In the spermatids of certain insects it was observed that in some

14

INVEETEBEATA

CHAT1.

FIG. 6.— Second matura-

cases there was one more chromosome than in others. Let us denote
these numbers by the formulae x and x + 1. Further investigation

i/ O

revealed the fact that this extra chromosome, termed the accessory
chromosome or hetero-chromosome, does not pair with any other
chromosome before the first maturation division : in this division it
divides longitudinally into two, whilst in the second maturation
division it does not divide at all, but passes to one pole of the spindle,
and is thus distributed to one of the two sperinatids resulting
from that division (Fig. 6). All the >ripe eggs showed a number of

chromosomes equal to the number in those
spermatids which had the extra chromosome.

The zygotes which resulted from the con-
jugation of these eggs with the two kinds of
spermatozoa would show therefore 2 x + 2 and
2 x + 1 chromosomes in their nuclei. Examina-
tion of the tissues in the adult insect showed
that the dividing nuclei of males possessed
2 x + 1 chromosomes, whilst those of females
had 2 x + 2 chromosomes. It seemed, therefore,
probable that in the case of these insects, this
abnormal chromosome contained some material
which determined the production of the female
tiou division of the sex in the zygote to which it passed.

male germ cells of Jn o{;her cages ft wag foun(j. that the

Protenor belfraaei. ±- i ^^ • i i 11

(After Wilson.) spermatius all contained an abnormal chromo-

h, Accessory chromosome. some, but that this abnormal chromosome was

in some spermatids large and in others small.

It was shown that in the spermatocyte of the first order both
abnormal chromosomes were present in the same nucleus, and that
they both divide in the first maturation division by longitudinal
splitting ; but that before the second division they fuse together to
form a bivalent chromosome, and that in
the second maturation division they again
separate from one another, and that one
proceeds to each daughter nucleus ; so that
in the case of these chromosomes alone the
second maturation division is a "reducing
division," whereas in the case of all the
others the first maturation division is the
reducing division. These abnormal chromo- FIG. 7.— Second maturation
somes are termed idiochromosom.es (Fig. 7). division of the male germ

When two idiochromosomes are present,
the developing eggs always carry the larger
one when maturation is complete, and the
nuclei in the tissues of the adult female have
two large special chromosomes ; whereas the nuclei in the tissues
of the adult male carry one large and one small idiochromosome.
Hence it is evident that the female grows from a zygote which has

cells of Euschistus

In /-is. (After Wilson.)

•'nil, the small idiochromosome ;
ill-, the large idioehromosome.

I INTRODUCTION 15

resulted fruin the fusion of an egg with a spermatozoon which
contained the larger idiochromosome ; the formula of its nuclei
therefore will be 2x + 2a, where a denotes the large idiochromosome.
The male on the other hand has developed from a zygote which has
resulted from the fusion of an egg with a spermatozoon containing
the .small idiochromosome, and the formula of its nuclei will be
2-x + a + b, where b denotes the small idiochromosome. Hence the
presence of two a chromosomes in the zygote determines the formation
of a female, and we can reduce the case of idiochromosoines to that
of the hetero-chromosome by 'supposing b diminishes until it dis-
appears altogether.

Other modifications have been described by Wilson ; thus a may
be represented by a group of chromosomes, but this group acts as
a unit in the reducing division and passes to one of two daughter
spermatocytes. The principle therefore is the same, and Wilson, in his
final summary, suggests that what determines a zygote to be a female
is an excess of peculiar trophic chromatin in its nuclei. Whilst a zygote
which is characterized by a defect in this regard becomes a male.

No such clear cases of differences between the sexes in the
number of chromosomes have been found outside insects. Many
statements as to the existence of such a dimorphism in other groups
have been made but have not been proved to be true. It is quite
obvious that such a dimorphism can only be demonstrated where the
number of chromosomes is few and easily counted, and that where
they are numerous the matter must remain in doubt.

It is clear that the existence of special sex-determining chromo-
somes is irreconcilable with Weismann's conceptions of the chromo-
somes as bundles of equipotential "ids" closely resembling one another,
any one of which was able to direct the whole development.

But the discovery of what Wilson calls sex-chromosomes has led
to other results of a far-reaching character. The reducing division
is a separation of whole chromosomes which immediately before this
had paired with one another. Now the idiochromosoines, when
present, always pair with one another, and the question arises whether
the pairing of the other chromosomes is not just as definite a matter
as that of the idiochromosoines. An examination of cases like the
germ cells of insects, where the number of chromosomes is small,
reveals the fact that in the nucleus, before "pairing" has taken place,the
chromosomes are of different sizes, but that there are always — except
in the case of idiochromosoines — two chromosomes of the same size,
and that these two pair with one another. The pairing therefore, and
the subsequent distribution of the members of the pair to different
gametes at the reducing division, is a definite and not a haphazard
phenomenon, and Montgomery (1904), to whom we owe this important
observation, has suggested that the two homologous groups of
chromosomes, which he asserts can be seen in all the nuclei of the
body, are derived from the male and female gametes respectively, to the
union of which the adult, which produces the germ cells, owes its origin.

16 INVERTEBEATA CHAP.

We thus reach the conception that male and female chromosomes
remain side by side without fusing in the nuclei of the offspring
during all its life, hut that when this organism in turn produces germ
cells these two kinds of chromosomes are segregated into different
gametes. Now this conclusion appears at first sight to accord exactly
with the theory to which the followers of Mendel have been led, and
it entirely destroys the second half of Weismann's theory of the pro-
duction of variations at the reducing division, by the casting out of
half the chromosomes, selected at random.

This brilliant school of " Mendelians," whose labours have been
summarized by their most brilliant member, Bateson (1909), have
been led to conclude that when two strains of animals are crossed,
the hybrid produces two kinds of spermatozoa, or ova, as the case
may be, one carrying the characters of the male and the other of the
female with respect to each differentiating character.

We should be wanting in our duty, however, if we allowed our
readers to imagine that Montgomery's theory had been fully estab-
lished. It is, on the contrary, only in the stage of a working hypothesis,
and it labours under many difficulties. Thus, its superficial agreement
with the Mendelian theory disappears under a deeper analysis. On
the idea that male and female chromosomes are distributed to distinct
gametes, each zygote should produce only two kinds of gametes
(leaving out of sight the sex-chromosomes for the present), one with
the maternal, one with the paternal characteristics. But the
Mendelian hypothesis demands two kinds of gametes with regard to
each differentiating character. Thus if a pea-plant have round and
green seeds, and if it be crossed with another having yellow and
angular seeds, we must expect the hybrid plants to produce seeds
which give rise to plants bearing yellow and green seeds, and round
and angular seeds ; but all the yellow seeds will not be angular nor
will all the green be round ; on the contrary there will be four
categories of seeds produced, viz. : — yellow round, yellow angular,
green round and green angular. It is not easy to see how Mont-
gomery's hypothesis can be fitted in with this breaking up of the
parental hereditary potencies into factors which are distributed
among the germ cells independently of one another. Agar has,
however, pointed out that in the stage of zygonema, when the first
pairing takes place between chromosomes, there is opportunity for
the exchange of material between them, and that when they again
separate in the stage of strepsinema they may lie different from what
they were before the pairing took place.1

Montgomery's theory demands, further, the belief that the identity
of each chromosome remains unimpaired during the resting period of
the nucleus, when no trace of distinct chromosomes can be detected.

1 It has also been suggested that, previous to the reducing division, the bivalent
chromosomes, each of which (e.v hypothcsi) consists of a paternal and of a maternal chro-
mosome joined end to end, may not all he arranged so that their homologous ends point
in the same direction. If this were so, one gamete might receive one chromosome from
one parent and one from another.

i INTRODUCTION 17

Occasionally, it is true, the sex-chromosome remains distinct during the
resting period. We may imagine, by an act of faith, that the others
too retain their identity although we cannot see them, but it seems to
us that the only meaning which can be given to such an identity would
be the persistence of a centre for the synthesis of some special
sul istance. Lastly, it may be that in some cases sex is not irrevoc-
ably determined in the germ, but can be determined by feeding.
This at any rate has been asserted by Born (1881) in the case of
tadpoles — though his results have not passed unquestioned. Wilson
attempts to get over this difficulty by supposing that the sex-
chromosome is only one of the factors which determine sex.

Our final conclusion is that investigators have only touched the
fringe of an intensely interesting and important subject, and that a
great deal more research must be done before definite conclusions
can be arrived at.

The meaning of the process of fertilization has proved a fascinating
subject for speculation. That the union of the two nuclei is not per
se necessary for development, is proved by the experiments of Loeb
and his pupils, who have caused the unfertilized eggs of Echinodermata,
Annelida, and Mollusca to go through the early stages of their
development by increasing the salinity or alkalinity of the water in
which they lie, i.e. by immersing the egg in what is called a hyper-
tonic solution, or by causing the egg to form a vitelline membrane
by rapid treatment with butyric and similar organic acids. By
uniting these two methods, i.e. by first causing the egg to form a
membrane through treating it with butyric acid and then treating it
with a hypertonic solution, a close approach to normal development
may be attained.

The formation of the vitelline membrane is due, according
to Loeb, to incipient cytolysis, i.e. the peripheral protoplasm
breaks down, forming minute globules which cohere together so as to
form the membrane. Too long exposure to the acid causes the egg
to die, by a continuation of the same process until the whole cyto-
plasm is resolved into a mass of globules, but this process is arrested
by the action of the hypertonic solution. Therefore Loeb concludes
that the influence of the spermatozoon is primarily chemical ; in fact he
supposes that it carries into the egg a ferment, " lysin," which starts
the process of cytolysis, and also another substance which arrests
this process after it has resulted in the formation of a membrane.

Loeb himself and his pupils Godlewski (1906) and Kupelwieser
(1906) have shown that it is possible to fertilize the eggs of a Sea-
urchin with the sperm of a Crinoid, a Star-fish, and even of a
Mollusc. In these cases the resulting organism, as long as it lives,
resembles exactly the normal larva which would have resulted if the
egg of the Sea-urchin had been fertilized by its own sperm, and
betrays not the smallest trace of the hereditary influence of the
foreign sperm which was used to evoke development. But of course,
throughout the animal kingdom, offspring are as likely to resemble
VOL. i c

18 INVEKTEBKATA CHAP.

the male parent as the female, and there must come a point when
the hereditary influence of the male asserts itself. This, LoeL
suggests, is when the foreign chroniatin becomes dissolved and
spreads its influence through the cytoplasm.

Now the common experience of breeders, as collected by Darwin,
bears witness to the beneficial effect on the vigour of the offspring
which is gained by crossing two parents of slightly different strains.
Their experience, moreover, is, that in what is termed inbreeding,
that is, when the male is nearly related to the female in blood, the
resulting offspring exhibit weakness of constitution. In the case of
the higher plants, which have both kinds of germ in the same
individual, self-fertilization produces in many cases similar results.
This can be explained if we imagine that in the normal multiplica-
tion of the cells in a developing organism, starting from the zygote
and leading through many cell-divisions to the formation of germ
cells, the wastage of the original chromatin is not quite made good.

From experiments made on Protozoa we conclude that without
chromatin no assimilation or building up of fresh living material can
take place, and we can only imagine that the influence of chromatin
is exerted through the substances which it is constantly giving off
into the cytoplasm. Now if our assumption be just, the germ cells of
each generation should become more and more imperfect in their
chromatin equipment, and this imperfection should exhibit itself as
a diminution in vitality. Hence we conclude that the prime object
of conjugation is to maintain the vitality of the stock by adding
together two chromatins of slightly different kinds, which will
presumably not be deficient in the same places. On this view the
purpose of reproduction by unicellular germs would be to render it
possible for the two chromatins to be thoroughly mixed.

Herbst (1900) has started an egg to develop by using hypertonic
solutions and valerianic acid, and then, when the nucleus had divided
into two, he has fertilized the bicellular organism with spermatozoa.
As a result, one of the two nuclei has conjugated with the sperm
nucleus, and an organism was produced, on one side of purely
maternal character and on the other side showing the paternal
influence.

It has been asserted in contradiction to this that there are some
plants, such as the Pea, which normally fertilize themselves and yet
undergo no deterioration, and others like Hieracium, the hawkweed,
in which sexual reproduction has been entirely replaced by asexual.
But such isolated cases cannot be allowed to weigh in the balance
against the great mass of evidence which tells in the contrary
direction. The deterioration due to inbreeding may be very slow
in showing itself, and a cross at long intervals may be sufficient to
restore vitality ; and he would be a rash man who would deny this
possibility in the case of any of the species which apparently undergo
continuous self-fertilization.

Leaving now the question of the meaning of the sexual element

i INTRODUCTION 19

in development, and turning to the developmental process itself, we
find that every animal passes through two phases in its passage to
the adult form. In the first of these phases the young organism is
sheltered from external influences either by an egg-shell or by the
body of the parent, or by both. Its food is supplied in the first
instance by the deuteroplasm or food-yolk embedded in its own
substance, supplemented in many cases by maternal secretions. In
the second phase the young animal, after escaping from its shelter,
is obliged to seek its own food, but it never is exactly like the
parent, and some time elapses and considerable growth takes place
before it attains the adult form. In the first phase it is known as
an embryo, in the second as a larva.

In different life-histories the embryonic and larval phases vary
enormously in their relative lengths. Sometimes, as in Echinoder-
mata, the young organism is thrown on its own resources at an extra-
ordinary early period of development, a very long larval life
ensues, and the young animal is at first utterly unlike the parent.
In other cases, as in the case of Man, when the young organism leaves
the parent it resembles the adult in all essential features. In
such cases it is customary to say that the larval stage has been
omitted. But the practice of confining the term " larva " to cases
where the free-living young differ markedly from the parent is not
logical. The baby is very different from a full grown man, and so is
the young child ; for example, the proportions of the limbs are
markedly different, and a continuous series of stages can be found
between differences of this kind and differences as great as those
which divide the larva from the adult Echinoderm. We may assert
with confidence that all animals pass through first an embryonic and
then a larval phase of development, and nothing is gained by calling
a larval stage which closely resembles the adult a " brephic " or
" neanic " stage, as was originally suggested by Hyatt and has been
adopted by some English zoologists.

Of course, development goes on throughout both embryonic and
larval phases, and the form of the organism is constantly changing ;
but there is one great group of animals, the Arthropoda, in which the
organism is confined within a rigid envelope derived from its own
secretions, and in this case, for a definite period of time, the external
form appears to be unchanged; only when the dead envelope is burst
and cast off, do the internal changes which have been going on
manifest themselves in a change of form. Hence we can appropri-
ately speak of these periods of fixity of form as a series of larval
stages, or, as Sharpe (1895) has suggested, we might call them
instars. In other groups of the animal kingdom where this
rigidity of form does not obtain, there are, nevertheless, crises in
development when great changes take place very rapidly, accom-
panied in many cases by the casting off of portions of the body
of the larva. These crises are termed metamorphoses, and the
stages of quiet growth preceding and succeeding them are looked

20 INVEETEBEATA CHAP.

on as . stationary in comparison, and spoken of as larval stages or
instars.

Now a great deal of the interest in the science of embryology has
arisen from the fact that both the embryonic and larval phases of
development show features which have been interpreted as being a
reproduction of the characters of far-off ancestors of the species to
which the adult belongs. This theory is the so-called fundamental
law of biogenetics, and is summed up in the phrase, " The individual
in its development recapitulates the development of the race." If
this "law" can be substantiated the interest in embryology becomes
immense, it binds all the innumerable phenomena of development
into one coherent scheme, and opens the door to the hope that we
may yet be able to sketch the main history of life on the earth.

The direct evidence of this history, as contained in the fossil record,
takes us back only a short distance. In the lower Cambrian rocks
the great groups of Mollusca, Arthropoda, Echiuodermata, and
Brachiopoda are all as sharply marked off from one another as at
the present day, and since only hard parts are preserved, the all-
important " soft " parts which constitute the real living matter are
irrecoverably lost, and no trace is left of an organism except it
possessed some kind of skeleton. But an egg has many points of
resemblance to the simplest animals, the Protozoa, and if development
be really a recapitulation of ancestral history, then the whole of the
ancestral history of an animal, from the Protozoan stage to the
present, should be presented in outline in its life-history.

But although most naturalists would agree that a life-history
contains ancestral "elements," all would be emphatic on the subject
that it likewise exhibits many features which are purely secondary,
and in no way reflect the characters of ancestors. With these general
considerations the agreement stops. As the founder of the Naples
Biological Station has caustically remarked, it is a curious fact that
every'investigator is convinced that the type which he is studying has
a monopoly of most of the primitive features, and that other types are
secondarily modified. The endless wrangles about primitive and
secondary features, which have made up so much of embryological
writing for the past forty years, have so disgusted many leading
workers in this field, that they have been inclined to go in the
opposite extreme, and deny altogether the "biogenetic law." Driesch
may be mentioned as an example of this, and a very searching
criticism of the whole hypothesis is given in the Darwin memorial
volume by Sedgwick (1909), who in former years had done more than
most workers to illuminate the hypothesis.

Driesch's (1907 and 1908) criticism leads him to the position that
the development of an egg into an adult is not to be explained by
physical and chemical laws, and he therefore attributes to each
species of animal a peculiar " entelechy " or soul, which presides over
the task of making its germs develop. Thus we are brought back to
pre-Darwinian days, to a position indeed more primitive than that

I INTBODUCTION 21

of the early nineteenth century, for it is surely easier to conceive of
an All-embracing Intelligence, Whose myriad plans were reali/ecl in
the different species, rather than of millions of uncaused and un-
related intelligences. Why, if the eutelechy of a Strongylocentrotus
be entirely distinct from that of an Echinus, should their products so
resemble one another? Has family resemblance in the animal
kingdom no meaning ? Our fathers attributed it to the Will of the
Creator. Darwin taught us to believe that it was due to descent
from a common stock. Driesch offers no explanation whatever, and
it seems to us that this final result is the reductio ad absurdum of his
whole system. Driesch's whole history has been that of the rebel
against accepted opinions, and in so far his intervention is healthy,
for nothing must be regarded as finally fixed, but pure reaction is
equally unjustified.

Sedgwick's position (1909) is different. He formerly accepted the
biogenetic law, but as its application seemed to yield the most dis-
cordant results, he has been led to undertake a critical examination
of the assumptions on which it is based. He points out that it is
tacitly assumed that when a new feature appeared in the history of
the race this showed itself only in the adult condition, whilst the
previous adult condition was retained as a developmental stage ; that,
in a word, as evolution has proceeded the life-cycle of living matter has
become more complex. Against such an assumption he points out that
a careful examination of the embryos of related species force us to the
conclusion that new features can appear at all stages of the life-history,
and that as all living matter known to us undergoes cyclical changes,
it is quite open to us to assume that this has always been the case since
the first appearance of living matter on the globe, and that therefore
the life-cycle has been modified but not extended. Neither of these
conclusions can be gainsaid a priori, and it is therefore time to take
stock of our data.

It would lead us altogether too far to discuss the general proposi-
tion that zoological affinity means blood-relationship: this, we take it,
has been abundantly proved by the evidence, which Darwin has col-
lected, of the relationship which breeds, varieties, and species sustain to
one another; if this be so it will be conceded that this zoological
affinity can be exhibited just as well by embryos as by adults, and
that, therefore, for the elucidation of biological affinity the study of
comparative embryology is necessary even if the biogenetic law be
baseless.

On looking into the question of the validity of this law, the first
question which presents itself for solution is the mutual relationship of
the embryonic and larval phases. On this subject Sedgwick himself
(1894) threw light some years ago, when he pointed out that the
embryonic phase is the remnant of a former larval phase, and that the
ancestral features which it exhibits are therefore features of a former
larva ; but these larval features, whether ancestral or not, consisted
of organs adapted to the larval mode of life. If, then, these features

INVEKTEBRATA CHAP.

were really ancestral, what was being reproduced were primarily
adaptations to an ancestral environment.

The proof that the embryonic stage is a concealed larval one exists
widespread in the animal kingdom. When we find that the Nauplius
stage of the shrimp Penaeus lives as a minute self-sustaining organism,
using the tiny hooks at the bases of its second and third appendages as
jaws to seize its prey ; and that the corresponding stage in the develop-
ment of the crayfish is passed within the egg-shell, but that the embryo
has the Nauplius limbs in the condition of useless stumps, although,
just as in the case of the free-swimming larva, the passage into the
next stage of embryonic life is initiated by a shedding of the cuticle,
then we have no doubt which is the more primitive, the larva or the
embryo. So too, when we find in the development of the Martinique
toad Hylodes that the embryo within the egg has the tail of a tad-
pole which is never used for swimming but is absorbed directly the
animal hatches, we have no difficulty in concluding that the original
condition of affairs was that in which the tadpole used its tail for
the purpose for which its shape is adapted.

Now the phase preceding the attainment of the adult form is
always larval (it is often termed brephic or neanic), and this,
according to the biogenetic law, should represent the last stage
which the race has passed through before attaining its present
condition, and will therefore be, generally speaking, the least modified
stage in the life-history, since it is the most recently added to the
series. Is there, then, evidence that this stage is of ancestral
significance ?

The answer to this question is that there is abundant evidence
of it, and a few instances of this may now be given.

The Oyster (Ostrea), contrary to the custom of the majority of bi-
valves, lies on one side, and remains fixed thus through life ; but the
American species, at least in its so-called "brephic" stage, when it has
terminated its free-swimming existence, creeps about for a short time,
and possesses, like other bivalves, a " foot," which is totally wanting
to the adult oyster.

Speaking broadly, when we examine the life -history of any
aberrant member of a well-defined group in the animal kingdom,
we find that in a late stage of its life-history it resembles the normal
member of the group to which it belongs. Portunion, an Isopod para-
sitic on Crustacea, ds distorted out of all resemblance to an Isopod,
but when young it is an unmistakable Isopod, a trifle simplified in
structure. The Crinoid Antedon when adult is devoid of a stalk,
and swims by muscular movements of its arms ; but when it is
young it possesses a stalk like the vast majority of its congeners.
The Plaice, Pleuronectes, swims with one side down, and both eyes are
twisted on to the upper side ; yet the larva of this fish has both sides
symmetrically formed with the eyes in the normal position, like the
vast majority of Teleostei. This list could be extended indefinitely,
and if the animals named are rightly classified in the groups in which

INTRODUCTION

23

they are placed, it is thereby implied that -they orice possessed the
normal features exhibited by the typical members of these groups ;
and therefore, beyond all question, their, late larval stages must be of
an ancestral character.

It follows, then, that advances in evolution do, as a rule, manifest
themselves when the animal is fully adult. But recent research in
the laws of heredity has rendered it almost certain that inheritable
variations are only those which affect the nature of the germ cell,
and most zoologists refuse to believe that the adoption of a new mode

B

FIG. 8. — The larva ami adult female of
Port union niai'nnilin. (After Giard.)

A, larva1 just hatched. B, adult female. aM, ab-
domen ; afl, anteunule ; ai2, antenna ; hr, brood-sac
composed of conjoined ovigerous plates of thorax ; <j,
jaws or gnathites ; h, head ; pi, swimmerets or pleopods.

of life by an adult could directly affect its germ cells. Lamarck's
idea that the change in the body induced by new habits could effect
a corresponding change in the germ cells is rejected by them. How,
then, is the adaptation effected ?

If an animal assumes a new habit or mode of life with success,
this can only be because a new and abundant food supply is thereby
opened up to it. Now Darwin has suggested that a rich food supply
is the proximate cause of the arrival of variations. Hence we may
provisionally assume that the new food supply upsets the stability
of heredity by altering the chemical constitution of the hereditary
substance in the germ cells, and so variations in all directions are

CHAP.

24 INVEETEBEATA

produced, and those variations are preserved which adapt the
organism at the right time to the new mode of life.

A

B

ctr-

FIG. 9.— The stalked larva and adult form of A ntuhni mullispina. (After P. H. Carpenter.)

A, larva. B, adult, 1>, Basal plate ; cir, cirrus ; jiin, pinnule ; /•', (irst radial plate ;
r2, second radial plate ; r'J, third radial plate.

If, then, the last stages in developmental history are, so to speak,

INTRODUCTION

25

the record of the last habits assumed by the species, the main frame-
work of all developmental history must be the condensed record of
ancestral experience ; for each stage in the development of an animal
bears the same relationship to the one which immediately precedes it as
the adult stage does to the last larval staije.

We must now consider some of the influences which modify the
ancestral character of developmental history. It is obvious that
there is no a priori impossibility that the supply of rich food should
produce variations which affect earlier stages of the life-history than

' '-

,.^x»i i, U i. I iiu H

an

pect

pcct

Fio. 10. — The larva and first metamorphosed form of the Plaice (Plewonectes platessa).

(After Cole and Johnstone. )

A, larva. B, young Plaice just after metamorphosis, an, anus; pect, pectoral tin.

the adult stage, especially if the alterations produced thereby have a
"survival value." Thus we may get secondary adaptations of the
larvae to their environment, which are seen to be secondary for the
reason that they differ widely from each other within the limits of
a group in which the adult structure is constant. When, for instance,
within the order of two-winged Hies we find some larvae adapted to
living in water, others to living in earth, others in dung, and still
others in dead bodies, and a few in living bodies, we cannot regard
any of these methods of life as ancestral, and we find that in each
case the larva is specially altered to suit it to the special conditions
of its existence.

26 INVEKTEBRATA CHAP.

The most widespread alteration iu the conditions of the larva
which is met with is its transformation into an embryo through its
retention within the egg-shell or the mother's body. Since, as a race
progresses from point to point in evolution, it should, according to
the " biogenetic " law, leave behind it a trail of larval stages, each
corresponding to a condition of life which had formerly been the
adult one, and in each of which the organism would have a distinct
method of obtaining its food and a special set of enemies, a very
long and complicated life - history should be produced. But the
dangers of such a long larval life are very great, therefore a great
advantage would be obtained by passing over some of these stages
within shelter, and, as was pointed out above, in all life-histories
we find an embryonic stage at the beginning.

Now the food necessary for development during the embryonic
phase is, in the vast majority of cases, furnished in the form of yolk
platelets, embedded in the cytoplasm. This yolk sometimes distends
the embryonic cells to enormous proportions ; it renders the process
of cell-division difficult, and sometimes even impossible. In the
ordinary process of cell-division each daughter nucleus becomes at,
and immediately after the time of nuclear division, the centre of an
attractive force which tends to collect the cytoplasm round it like
a ball. In some cases, in consequence of this force, the first products
of the division of the egg appear as spheres touching one another
only at a point. But this period of activity is succeeded by a period
of quiescence, and the centripetal force subsides^ so that the
cytoplasm of the two daughter cells tends to flow together again,
unless a cell membrane has been formed between them in the
meantime.

When yolk is present it impedes the action of the centripetal
force, apparently by rendering the cytoplasm less viscous ; for
cytoplasm devoid of yolk behaves like thick honey, whilst that
which is loaded with yolk behaves more like a mixture of honey
and water. Consequently, in yolky eggs we find that in the first
stage of their development they either divide into a few large clumsy
cells, or else that cell division is represented by nuclear division only.
Further, since the yolk is never uniformly distributed in the ovum, but
is usually massed at one side, the first divisions result in the produc-
tion of cells of unequal sizes or in the production of a cap of cells at
one side of the egg, the rest remaining unsegmeuted. The pole of the
surface of the egg which is relatively freer from food-yolk, and where
the division into cells first occurs, is termed the animal pole of the
egg; it is here too that the polar bodies are given off. The opposite pole,
where most of the yolk is accumulated, is termed the vegetative pole.

Such eggs are termed meroblastic, whilst eggs in which the yolk
is sufficiently small in amount to allow of the division of the whole
are said to be holoblastic. Further, whilst in most eggs the yolk is
massed at one side (telolecithal) (vide Fig. 3 A), in a wide range of eggs
it is massed at the centre, surrounded by a rind of comparatively yolk-

INTRODUCTION

27

free protoplasm (centrolecithal) (Fig. 11). The result of this latter dis-
tribution is that a skin of cells is formed over an inert mass of yolk.
But the clogging influence
of yolk extends far beyond
the first stages of develop-
ment.

The course of development
can indeed be roughly divided
into three stages : — (1) In
the first the zygote becomes
divided into a number of em-
bryonic cells or blastomeres ;
this stage is called segmen-
tation ; (2) in the second
these cells are arranged so as
to form the primary organs,
the so-called germ layers, i.e.
the skin, and the lining of the
gut and of the body cavity ;
this stage is called the forma-
tion of the layers ; and (3)
in the third stage these layers
are modified into the larval or

y-

n

FIG. 11. — Unripe egg of Limulus polyphemus.
(After Munson. ) All example of a centro-
lecithal egg.

permanent organs ; this last
stage is called organogeny.

ch, chorion ; g.s, nucleolus (germinal spot) ; g.v,
nucleus (germinal vesicle); per, peripheral cytoplusmic
area free from yolk ; y, central area of cytoplasm filled
with yolk ; //.n, yolk nucleus.

Eggs with little or no yolk
are termed alecithal (Fig. 12). If yolk in the form of refringent
globules should be totally absent, reserve stuffs in the shape

of masses of chroiuatm are scattered
about through the cytoplasm. In such
e<)>o'S the building up of organs out of

OO D J. O

the first cells, or blastomeres which
result from division, takes place by the
simplest processes of unequally rapid
growth of different parts, and of folding.
Now in the folding of a layer of cells it
is essential that" the radius of curvature
should bear such a relation to the size of
the individual cell that the latter should
not be deformed. When the layer consists
of a few large yolky cells, folding becomes
( After Schaxei.j An example impossible and is replaced by proliferation

FI v •% 't. * «*> ^ Y''

FIG. 1'2. — The ripe egg of
Strongylocentrotus lividus.

of an alecithal egg.

of new cells at one point in the layer.

• /(/, deposits of chromatin scat- Food, as W6 have SCCll, is USlially

supplied to the immature ovum by the
sacrifice ol the less fortunate oogoma or

immature ova. In the case of the common polyp, Hydra, the im-
mature egg comes at this stage to resemble an Amoeba. But in one

28 INVERTEBKATA

CHAP.

or two groups of animals the immature eggs destined to destruction
are supplied to the zygote or fertilized ovum to be used as food.
This leads to the strangest modifications of the early stages of
development. The cells which result from the first divisions of the
zygote may actually separate from one another and come together
again in such a way as to surround the follicle cells, and this has
led to the statement that, in certain cases, the egg dies and the
embryo is developed out of follicle cells, but there is apparently no
justification for this statement (cf. p. 635).

But an embryonic stage may be, so to speak, intercalated between
two larval stages. In the history of the race the change of habits
which is recapitulated in the life-history, must have been con-
tinuous, for no animal ever suddenly changed from one mode of
life to another. Now the dangers incident to larval life and the
opportunities of obtaining food, may vary very much, and will be
much greater in some stages than others. If in one stage a large
store of nourishment can be accumulated, it will be an advantage to
the animal to pass quickly over the next stage, which is probably less
favourable, and so we may get these intercalated embryonic, or, as
they are usually termed, pupal stages. During these the animal is
sometimes as quiescent as a true embryo, as in most insects ; in others,
such as Cirripedia and Holothuroidea, it is active but takes no food.

But there is one outstanding feature about m«st larvae which
strikes the observer, and that is their extremely small size compared
with that of the adult into which they eventually develop. This
reduction in size is in all probability a secondary modification, but it
has led to other modifications. An alteration of size produces an
alteration in the physiological relations of the organism, and we
find that where, from other evidence, we have reason to suspect that
the ancestor had a long series of similar organs, the larva may only
show one or two ; for all these organs, if reduced to the same scale
as that to which the whole body of the animal has been diminished,
would become physiologically ineffective. Take, for instance, the
gill slits in the larva of Ampliioxus. These must have a certain
minimum size if they are to work, on account of the viscosity of water,
and therefore whilst they remain larger in proportion than the other
organs of the body, their number becomes diminished, and so where
the ancestor had almost certainly two rows of such slits, we find
them represented in the larva by one row of slits which occupy the
whole ventral surface.

Lastly, it may be remarked that whereas it is true, generally
speaking, that the more primitive features an adult exhibits, the
more primitive features are found in the larva, yet the change from
the larval to the embryonic method of development seems to take
place quite independently of the status of the adult, and some
animals preserving very primitive features have a development
almost completely embryonic, whilst others higher in the scale retain
a long larval history.

I INTRODUCTION 29

If it be asked why all animals have not exchanged the larval for
the embryonic type of development, considering the advantage which
the embryonic phase possesses, from the point of view of the safety
of the young organism, it must be pointed out that the larval form
of development offers compensating advantages from the point of
view of wide dispersal of the species. The balance between these two
alternatives seems to have been easily inclined one way or the other.

It is therefore of the essence of Comparative Embryology to
separate the fundamental ancestral traits of development from the
superficial and secondary, and this is the task that has been patiently
pursued for the last thirty years. As Sedgwick has pointed out, its
results have been highly disappointing, and this has led many to doubt
the validity of the ancestral explanation of development. But the
reason for this disappointment is largely a human failing which will
lead to equal disappointment in any branch of science. This human
failing is the ardent desire to settle fundamental questions in a few
years. Obviously the most difficult pages of the embryonic record to
decipher would be the earliest, for these have suffered most secondary
modification, and yet it is precisely over such questions as the first
differentiations of the embryo, such as the formation of the primary
tissues or so-called " layers " of ectoderm, endoderm, and niesoderm,
that most of the divergences of opinion have arisen.

When we allow the mind to contemplate the vast profusion of
living species at present in the \vorld, each with its own peculiar life-
history, and then reflect how few are at all known, we can see at
once how small a clearing we have made in the forest of comparative
embryology, and how premature it is to abandon the hope of finding
a law underlying the likenesses and unlikenesses of the various
modes of development. Where, as in the case of Vertebrata, the
knowledge is more complete than in the case of other groups, the
recapitulation of the structure of the lower members of the group in
the young stages of the higher, is so plain as to be obvious to all.
When the knowledge of other groups becomes equally complete the
same thing will be obvious there also.

Those who have abandoned Comparative Embryology for Experi-
mental Embryology have set themselves the task of finding out the
mechanism of the transformation of the apparently formless egg into
the differentiated adult. But here again the impatience with delay,
the determination to arrive at "basal" principles at once, will prepare
disappointment for the workers in this branch also.

Thus we find, as already pointed out, that whilst Driesch arrives
at the conclusion that each kind of life-history owes its peculiarities
to a non-material entelechy — but leaves the resemblances between
the life-histories utterly unexplained, Herbst arrives at the con-
clusion that in each stage of development a substance is found which
acts as a " stimulus " to cause the development to the next stage,
while Loeb on the other hand maintains that until the conception of
" stimulus " is utterly abandoned no real progress with the subject

30 INVERTEBKATA CHAP.

will be made. Here we have divergences as great as those which
exist between any upholders of rival phylogenetic theories.

The real truth is that Experimental Embryology is an adjunct
and not an alternative to Comparative Embryology. It is a new and
refined instrument of dissection : instead, for instance, of separating
the blastonieres of a segmented egg by optical differences they are
actually separated and their values tested by their powers of develop-
ment. But the difference between the Echiuoderm egg where any of
the first eight blastouieres will develop into a whole larva, and the
Annelid egg where the loss of a blastomere means the loss of a portion
of the larva, still requires for its explanation the principle of affinity,
that is to say that the ultimate explanation of the specific peculiarities
of development is found in the chemical nature of the hereditary
substance.

So, before the future student of embryology stretches an almost
limitless field of research. We must ultimately find out not only
how the chemical quality of the germ-plasm determines the growth of
the formless egg into the highly complex adult, but we must also find
out how this chemical quality can be altered, so that variations can occur
and evolution can take place, and this is the root-problem of biology.

In order to make any attempt to solve this root problem we must,
however, be able to control the whole life-- cycle of the animal
experimented on, and this is precisely where the work of Loeb,
Herbst, and Driesch breaks down. All these workers have chosen as
experimental objects the eggs of Echinoderms. These eggs are
produced in enormous numbers and are easy to rear through the first
stages of their development, but to reach even the adult form — to say
nothing of the adult dimensions — they have to pass through a
prolonged larval life during which there is an enormous mortality,
and even when this metamorphoses into the adult shape is success-
fully accomplished they have less than the millionth of the bulk of the
fully ripe sexual form. Under the most favourable circumstances a
year or two must elapse before they could produce germs and, therefore,
before it could be possible to say whether the experiments had really
altered the hereditary potentialities, or whether the distorted larva
is merely the resultant of the new force applied and of the unaltered
hereditary potentiality of the germ. The method of rearing these
larvae until they attain sexual maturity has now been elucidated, but
only a small proportion of the fertilized eggs can so far be reared ; and
none of the workers mentioned above have attempted to rear the
larvae beyond the earliest stages of their development.

We pass now to consider the special embryology of the different
groups of Invertebrata. In every case we shall, so far as possible, give
examples of the fundamental laws of development laid down in this
introductory chapter, and we shall indicate also what solid results
have been gained from experiments performed on the developing eggs
of animals belonging to each group.

The group Protozoa are excluded, not because they do not

I INTRODUCTION 31

in many cases exhibit a development showing larval and embryonic
stages, but because in most cases it is not easy to determine what
corresponds to the adult stage in Protozoa, and their life-histories are
too imperfectly known for profitable comparison.

LITERATURE

Most of the works contained in this list are of the nature of summaries or text-books,
in which full reference to all the earlier works on the subject will be found.

Agar, W. E. The Spermatogenesis of Lepidosiren paradoxn. Quart. Journ. Micr.
Soc. vol. 57, 1911.

Bateson, W. Mendel's Principles of Heredity. Cambridge, 1909.

Born. Experimentelle Untersuchungen iiber die Entstehung der Geschlechtsunter-
schieden. Breslaner artzlicher Zeit., 1881.

Conklin, E. G. Karyokinesis and Cytokinesis in the Maturation, Fertilization, and
Cleavage of Crepidnln and other Gastropoda. Journ. A.N.S. Phila. vol. 12, 1902.

Darwin, C. The Variation of Animals and Plants under Domestication. London,
1868.

Driesch, H. The Science and the Philosophy of the Organism. Gifford Lectures.
Aberdeen, 1907 and 1908.

Duesberg, J. La Spermiogenese chez le rat. Arch. Zellforsch. vol. 2, 1909.

Godlewski, E. Untersuclmngen iiber die Bastardierung der Echiniden- und
Crinoidenfamilien. Arch. Ent. Mech. vol. 20, 1906.

Herbst, C. Vererbungsstudien V. Ibid.

Hertwig. Vergleich der Ei- und Samenbildung bei Ascaris megalocephala. Arch.
Mikr. Anat., vol. 36, 1890.

Kupelwieser. Entwicklungserreguug bei Seeigeleier durch Molluskensperm.
Arch. Ent. Mech. vol. 22, 1906.

Loeb. Die ehemische Entwicklungserregung des tierischen Eies. Berlin, 1909.

Montgomery. Some Observations and Considerations upon the Maturation-phen-
omena of Germ Cells. Biol. Bull. vol. 6, 1904.

Schaxel, J. Das Zusammenwirkung der Zellbestandteile bei der Eireifung, Furchung
und ersten Organbildung der Echinodermen. Arch. Mikr. Anat. vol. 76, 1911.

Sedgwick. On the Law of Development commonly known as Von Baer's Law, and
on the Significance of Ancestral Rudiments in Embryonic Development. Quart. Journ.
Micr. Sci. vol. 36, 1894.

Sedgwick. The Influence of Darwin on the Study of Animal Embryology. Darwin
and Modern Science. Cambridge, 1909.

Sharpe. Insects. Camb. Nat. Hist. vol. 5, 1895.

Shearer. The Problem of Sex Determination in Dinopliilus gyrociliatus. Quart.
Journ. Mic. Sci. vol. 57, 1912.

Weissman. Die Kontinuitat des Keimplasmas als Grundlage einer Theorie der
Vererbung. Jena, 1886.

Weissman. Das Keimplasma, eine Theorie der Vererbung. Jena. 1892.

Wilson, E. B. The Sex-Chromosomes. Arch. Mikr. Anat vol. 77, 1911.

CHAPTER II
PEACTICAL HINTS

THE object of this book is not merely to lay before the reader the
best ascertained results of embryology, it is also designed to
indicate the directions in which further research may be most ad-
vantageously prosecuted, and to suggest reliable methods of pursuing
such researches. Incidentally defects in the methods employed by
some investigators, and the possible bearing of these defects on their
results, will be pointed out.

In the present chapter 'some general instruction will be given on
methods of procedure which are applicable to all, or nearly all classes
of embryo, while special methods will be described when each separate
phylum is described.

When one endeavours to work out the life-history of an animal
the first step is to observe the larvae or embryos in the living state.
In many cases a large number of points can only be made out in the
living embryo, since the tissues are then in their natural state of tur-
gescence, and living protoplasm is relatively transparent. The next
step is to preserve or fix the embryos, dehydrate and clear them and
mount them whole.

Fixing or preservation consists in adding some reagent to the
specimen to be preserved which will form a stable and more or less
solid compound with the protoplasm of the organism. This compound
enables the form of the organism to be retained during the process of
dehydration, and the macerating and deforming effects of the diffusion
currents produced in this process to be resisted. Dehydration, is
the removal of the water by successive immersion of the object in
different grades of alcohol ; clearing, is infiltration of the tissues by
an oil like oil of cloves, cedar oil, etc., which renders them transparent.

Now the reagent which forms the strongest compound with
protoplasm and preserves in it the nearest resemblance to its living
condition is the solution of osmium tetroxide in water, usually
erroneously called osmic acid. For effective fixation a solution of at
least '25 per cent must be used. "Osmic acid" has two disadvantages,
it produces a very black stain which consists of the metal osmium,
and it is apt to render the tissues brittle. Further, if applied to objects

32

CHAP, ii PRACTICAL HINTS

of any size osmic acid forms a crust of hardened imperviable proto-
plasm which prevents the penetration of the reagent into the interior.
It is, therefore, a reagent eminently suited for the preservation of
minute larvae and the permeable tissues of calcareous sponges.

For the denser tissues of siliceous sponges other reagents would
be more suitable ; such, for instance, as a mixture of 3 parts
concentrated solution of corrosive sublimate in water and 1 part
of glacial acetic acid. This is one of the best and most universally
employed preservatives : many investigators use, however, a smaller
proportion of acetic acid (often as low as 5 per cent) than that just
mentioned ; it is to be remembered that acid reagents are unsuitable
for calcareous sponges and for other organisms which contain much
calcareous matter, because the evolution of carbonic acid gas dissolves
the calcareous matter, and so causes the formation of blebs in the
tissues and of artificial rents and cavities winch have no counterpart
in the living animal. When it is desired to decalcify, this is best
accomplished when the organism is in strong alcohol. If a drop
or two of nitric acid be added to a small bottle (of two fluid ounces)
full of strong alcohol and well shaken, a solution is produced which
will decalcify so slowly that the resulting gas is at once dissolved and
never forms bubbles.

A different method of decalcifying organisms which have been
preserved in osmium tetroxide may be mentioned here. If, after
being blackened by immersion in the solution and then rinsed in
clean water, the specimens be immersed in Miiller's fluid, not only
will the calcareous matter be slowly removed but also the excess of
metallic osmium, and the tissues will be rendered less brittle.
Miiller's fluid is a mixture of bichromate of potash, which contains
unsaturated chromic acid and sulphate of sodium. Flemming's
fluid, which is a very favourite preserving medium, is really an
attempt to combine the advantages of osmium tetroxide and chromic
acid, for it is a mixture of these two fluids with acetic acid. It is an
excellent preservative, but is intensely acid and open to the same
objections as other acid reagents. The same remarks apply to
Hermann's fluid, which is a mixture like Flemming's fluid, in which
acid platinic chloride replaces the chromic acid.

When it is desired to make whole mounts of minute forms it
will generally be found that osmium tetroxide, corrosive sublimate,
etc., render them too opaque. Strong formalin — that is a 40 per cent
solution of the gaseous formic aldehyde in water — is a splendid
reagent for this purpose. It kills small larvae instantaneously, with-
out any shrinkage. It is apt, however, to become acid by the oxidation
of the aldehyde into formic acid ; it is therefore advisable to carefully
neutralize the solution before employing it. Further, the compound
which it forms with protoplasm is soluble in water. Therefore, after
a few minutes' sojourn in the formalin solution, the specimens must
be instantly transferred to absolute alcohol, and in this they must
be stained. Eosin or methyl green dissolved in absolute alcohol are
VOL. i D

34 INVERTEBRATA CHAP.

very good stains. The transference to oil of cloves must be made by
adding this substance drop by drop to the absolute alcohol at intervals
of an hour or so for several days. After a sojourn in the pure oil
the specimen is placed in the concavity of a hollowed slide and
suddenly covered with thick solution of Canada balsam in xylol.
The oil of cloves flies to the periphery of the balsam owing to
surface tension and may be removed by blotting-paper.

When all the information possible has been gleaned from whole
mounts of embryos and larvae the next step is to cut them into
series of sections arranged in order, but for this purpose they must lie
embedded in a block of paraffin so that the sections when cut by the
microtome will lie parallel to a known direction. To accomplish this
placing, or orientation, as it is called, in the case of minute larvae is
a matter of great difficulty, and unless the sections are cut in the
right direction they are very difficult to interpret. The best way to
overcome this difficulty is to embed the specimens in celloidin
before embedding in paraffin. The solution of celloidin used for
embedding vertebrate tissues, consisting of celloidin dissolved in
a mixture of equal parts of absolute alcohol and ether, is not
suitable for delicate larvae because too violent diffusion currents
are produced in the process of changing from alcohol to the
celloidin solution. If, however, the celloidin be dissolved in a
mixture of four parts of absolute alcohol and one part of ether,
then such currents are avoided. It is well to have three grades of
this solution, one saturated, one made by diluting the saturated
solution with an equal bulk of the solvent, and one by diluting it
with two volumes of the solvent. The objects, if they are small,
should remain in each grade for about one day. Then the thick
solution with its contained embryos is poured into chloroform and
the celloidin hardens to a cheesy consistence. After an hour's
sojourn in this fluid a piece of celloidin containing the embryo
can be cut out and embedded in paraffin.

The embedding may be done in one of two ways.

(1) The piece of celloidin containing the object is placed in
absolute alcohol, to remove any trace of moisture, and then
immediately transferred to fresh chloroform to which fragments of
clean paraffin are added. If the whole be heated to 60° for an
hour all the chloroform will have evaporated and the object can now
be poured, together with some of the paraffin, into a mould and
allowed to cool. Before transferring to the mixture of chloroform
and paraffin, the object can be studied under the lower power of the
microscope and the celloidin shaped so as to direct the orientation of
the block of paraffin.

(2) The object and its surrounding celloidin may be transferred
to cedar oil. If this lie warmed for half an hour (by being placed on
the top of the thermostat) all traces of moisture will be absorbed,
and the cedar oil will render the celloidin absolutely transparent,
so that the object can be examined as if it were mounted in oil of

ii PEACTICAL HINTS 35

cloves. The celloidin should then be cut as before so as to indicate
the position of the object, and the latter, in its celloidiii block,
should be transferred to a mixture of cedar oil and hard paraffin
and heated to 56° for fifteen minutes, and then for fifteen minutes
to a bath of pure hard paraffin.

This second method has the disadvantage of rendering the
embryonic tissues rather brittle, but one great advantage of
embedding in celloidin is that the tissues of the embryo become
penetrated while cold by a substance which hardens and gives them
support, before they are subjected to the ordeal of the hot paraffin
bath, which has a tendency to cause shrinkage.

When the sections are cut they are best mounted by first
smearing the slide with Mayer's glycerine and albumen fixative,
then laying the sections upon it and adding a layer of water heated
to 60° ; the hot water cools at once to about 45°, and this heat
will flatten out the sections without melting the paraffin. The water
is drained off and the slide dried on the top of the thermostat for
forty minutes. Then the paraffin can be melted off and washed off
in xylol. It should then be immersed in oil of cloves for one minute,
which softens and dissolves the celloidiii. Then it should be placed,
not in absolute alcohol, but in 90 per cent alcohol, which washes off
the oil of cloves and at the same time removes the glycerine from the
glycerine and albumen fixative; it finally coagulates the latter and also
hardens the semifluid celloidin, so that it forms an additional fixative
for securing the adhesion of the sections to the slide. Another
method is to transfer the slide from pure xylol to a mixture of equal
parts of xylol and absolute alcohol. The absolute alcohol coagulates
the albumen and removes the glycerine. The slide can then be
transferred to 90 per cent alcohol and thereafter to alcohol of lower
grades. Sections thus fixed will stand any further treatment without
becoming loose.

Mayer's fixative is made by mixing white of egg strained through
muslin with an equal volume of glycerine. A few drops of thymol
are added to prevent the decomposition of the albumen.

In staining objects which have been preserved in osmium
tetroxide it is often found that the black deposit of metallic osmium
in the tissues prevents the stain from taking effect. The best
general stain is Grenadier's (some times called Delafield's)haematoxylin.
This is best used in a solution made by diluting the concentrated
stain in three or four times its bulk of distilled water. This solution
should be filtered before being employed. If the sections be
previously immersed in a solution of borax-carmine in 70 per cent
alcohol it will be found that they can remain in it for 24 hours
without absorbing any stain, but if then they be transferred to the
solution of haematoxylin described above, they stain rapidly and
well. Excess of stain is removed by immersing the sections in a
solution of acid alcohol made by adding two drops of strong
hydrochloric acid to 100 c.c. of 70 per cent alcohol. If the

36 INVERTEBRATA CHAP. 11

sections be examined from time to time under a microscope as
the staiu is being removed, a point will be detected at which
the whole section takes on a reddish colour, and the nuclei stand
out prominently. When this is observed the sections should be
washed free from the acid alcohol by immersing them in *70 per
cent alcohol. They should then be held inverted for a few moments
over the mouth of a bottle of strong ammonia, the escaping fumes
from which neutralize the last traces of acid, and the sections, now
of a beautiful blue colour, may be dehydrated and mounted. The
different tissues yield up their stain in different degrees, and a
beautiful differentiation is effected by the different tints of blue.

If a double stain be desired it can be effected by finally dehydrat-
ing the sections in absolute alcohol to which eosin has been added,
but if they remain too long in this solution all the haematoxylin
will be washed out.

The methods described in this chapter are general methods
applicable to all classes of embryos ; special methods will be described
in the chapters dealing with special groups.

CHAPTER III
POKIFERA

Classification adopted —

(Homocoela ( = Asconidae)

|» o 1 n Q y» A o F ^ '

(Heterocoela fyconidae

( Leuconidae

Triaxonia ( = Hexactinellida)
Demospongiae

THE group Porifera or Sponges stand apart from all the rest of the
Metazoa, and their embryology is consequently of very great interest.
We may suggest as a form for practical study the development of the
Calcareous sponge Grantia compressa.

This sponge, distinguished by its flattened shape, is a common
denizen of the British coasts, and its embryology is being worked
out by Professor A. Dendy. Allied species occur on the coast of
North America ; and the course of its development, so far as deter-
mined, so closely resembles that of the Mediterranean species, Sycandra
raphanus — the subject of Schulze's classic research (1875) — that the
latter may be taken to represent that of Grantia and of Calcarea
generally.

SYCANDRA RAPHANUS

The eggs are found embedded in the jelly which forms the sub-
stance of the wall of the sponge, intervening as it does between the
cells forming the dermal membrane and those lining the paragaster
and the extensions of this latter cavity into the flagellate chambers.
The spermatozoa occupy a corresponding position in the male. When
ripe, they bore their way through into the flagellate chambers, and
are discharged by the osculum. They swarm in the surrounding
water, and, coming under the influence of the inhalent currents of
the female, they penetrate through its pores and thence find their
way to the eggs, which are thus fertilized in situ.

The fertilized egg undergoes the first stages of its development in
the maternal tissues. It is found to be contained in a cavity Lined

37

38

INVEKTEBEATA

CHAP.

by a definite layer of dermal cells. This cavity is wedged in between
the layer of dermal spicules and a flagellated chamber. As it

v O

enlarges to suit the size of the growing embryo, it encroaches on the
cavity of the flagellated chamber, since the layer of dermal spicules is
unyielding. (Dendy, 1889.)

The first stages of development must therefore be studied in
transverse sections of the adult.

When the larvae emerge they must be encouraged to settle on
some convenient portable object. If it is desired simply to make

whole mounts, the bottom of the vessel in
which the parents are contained is strewn
with coverslips, and these are removed when
the young sponges have attached themselves
to them, and immersed in 1 per cent solu-
tion of osmic acid till fixation is effected,
then stained in picro-carmine and mounted
whole. If it is desired to cut sections of the
larvae, the coverslips must be covered with
a layer of paraffin wax or photoxylin, which
can be scraped off and the larvae thus
removed, when they can be dealt with
by the methods described in the previous
chapter.

The egg divides into two, four, and eight
blastomeres, which are arranged in one plane,
and, from the 4-cell stage, they surround a
central cavity open at both ends, which owes
its existence to their mutual separation
(Fig. 13). This stage is followed by a division
of all the cells into two tiers, so that sixteen
cells are formed in two rows, and then each
of these rows is subdivided into two further
rows, and so we reach the 32 -cell stage.
Divisions now follow one another in the
individual cells somewhat irregularly, and
thus an oval vesicle is constituted, which
may be termed the blastula, one pole of
which is rounded and one flattened, whilst inside it there is a cavity
which is a development of the cavity formed by the separation of the
first segments of the egg, and which is termed the blastocoele.

One opening of this cavity to the exterior, that at the pointed
end, is by this time closed, but that on the flattened " basal " surface
persists for some time, though it too eventually closes. The, cells
immediately surrounding this latter pore are distinguished from the rest
by becoming extremely granular. The granular cells increase by
division to thirty-two, whilst the remaining cells become extremely long
and columnar, and each develops a flagellum. The columnar half of the
embryo is pressed against the wall of the yielding chamber, but the

FIG. 13. — Two stages in the
segmentation of the egg
of Sycandra raphanns.
(After Schulze.)

A, 8-cell stage in which all the
blastomeres are in one tier with
a central aperture. B, 16 -cell
stage blastomeres arranged in
two tiers of eight each round a
central aperture.

Ill

POKIFEKA

39

granular cells encounter the resistance of the spicnles, and therefore
the embryo becomes hat-shaped. A few small cells are found in the
segmentation cavity. Dendy (1889) thinks that these cells, which
may be termed mesenchyme, have been budded from the flagellated
cells, but this is not certain. The granular cells now proliferate
rapidly, especially in the centre, and form a thick mass which

becomes invaginated into the blastocoele.

The embryo is now ready
for birth. By the activity
of its flagella it bores its way
into the adjacent flagellated
chamber of the mother, and
then escapes through the
osculum. During this pro-
cess the blastocoele seems to
absorb water, the invaginated
cells are exserted, and thus
the free -swimming larvae
acquire an oval form; but

CO.

Flu. 14. — View of the embryo of Gran fin lubi/rinthica
in the blastula stage lying in the embryonic
chamber of the mother. (After Dendy.)

col, collared cells lining a maternal flagellated chamber ;
etrib, embryonic chamber ; gr, granular cells of the embryo ;
ines, cells, so-called mesenchyme budded into the blasto-
coele ; spic, maternal spicules.

FIG. 15. — View of the embryo of
Grantia labyrinthica in a later
stage of development than that
represented in Fig. 14. (After
Dendy. )

Letters as in Fiic. 14.

the cells forming one half of the wall of this vesicle are granular and
rounded, whilst those forming the other half carry long flagella, and
possess, in addition, a bright red pigment. The interior is half-tilled
up with granular cells. Such a larva is termed an amphiblastula, and,
as we shall see, this type recurs in all families of sponges (Fig. 17).

After swimming for a day or two the amphiblastula comes to rest
on the surface of a smooth stone, its ciliated half which preceded the
other whilst the larva was moving, being directed downwards.
Within a few minutes the larva has undergone an entire change of
shape. Its anterior end flattens out; the ciliated cells which con-

FIG. 16. — Section of a portion of Grantia labyrinthica. (After Dendy.)

Showing the escape of the larva from the tissues of the mother sponge into the flagellated chamber
of the mother ; /, flagellated chamber ; I, escaping larva ; o, opening of flagellated chamber into central
cavity (paragaster) of sponge.

Flit. 17. — The Amphiblastula larva of Grantia labyrinthica. (After Dendy.)

ft, flagellated cells ; gr, granular cells.

40

CHAP. Ill

POEIFERA

41

stitute it become invaginated into the posterior half, and the blasto-
coele is thus reduced to a mere slit. The cells forming the edge

B

gr

FIG. 18. — Two stages in the fixation of the larva of »s>'//<''"'"'m ritjilnnnts. (After Sehulze.)
A, the flagellated cells are just retreating into the interior. B, the larva lias assumed the form of a
hemispherical cup and is attached by amoeboid processes of the outer granular layer. Seen in optical
section, fl, flagellated cells ; gr, granular cells ; ;i, porocytcs (?).

of the cavity of invagination are granular, and when the ciliated
cells become invaginated, these granular cells extend inwards

FK;. 19. — An early stage in the metamorphosis of the Ascon stage of Sycandra

into the adult. (After Maas.)

A, external view of young sponge. B, diagrammatic longitudinal section of the same to show the
gradual displacement of collar cells by granular cells. C, a small portion of such a section further
enlarged, r/i, radial flagellated chainber ; fl, flagellated cells; gr, granular cells (in C the reference
line points to a spot where the granular cells are migrating inwards) ; os, osculum ; p, inhalent pore ;
PU, paragaster.

along the substratum, and floor the cavity of the invagination
(Fig. 18); they also extend outwards in irregular tongue-like pro-

42

INVEKTEBRATA

CHAP.

cesses and adhere to the substratum ; the process of attachment of
the larva to the substratum is known as fixation.

The larva is thus converted into a closed cylinder, the wall of

FIG. 20. — A late stage in the metamorphosis of the Ascou stage of Sycandra raphanus
into the adult condition. (After Maas. )

Letters as in Fit;. 10.

which consists of an outer layer of flattened cells, and an inner layer
composed of ciliated cells, on each of which the collar soon makes its
appearance. This collar is characteristic of the cells lining the flagel-
lated chambers in all Porifera. Between the two layers a layer of

in PORIFEEA 43

jelly makes its appearance, which is the real stiffening element in
the sponge-wall.

The formation of inhalent pores is now begun. Individual cells
of the outer or dermal layer extend inwards through the jelly, and
press asunder adjacent cells of the inner or gastral layer. These cells
then become hollowed out, converted into drain-pipes, as one might
term it, and the action of the flagella draws in water through them.
Other cells migrate from the outer layer into the jelly, and form
the characteristic calcareous needles or spicules. The first type of
cells are called porocytes, the second scleroblasts. After the pores
have been acting for some time, an exhalent opening is formed at
the distal end of the cylinder. The formation of this osculum seems
to lie due in part to the hydrostatic pressure caused by the action of
the pores.

The tiny sponge is now quite comparable to the type of adult
sponge exemplified by the genus Leucosolenia. Its transformation
into the adult Sycon is an affair of slow growth, and the process has
not been observed in this Grantia, but there is no reason to doubt
that it is essentially similar to what occurs in Sycandra rapkanus,
in which it has been described by Maas (1900).

In Sycandra, pouches grow out horizontally from the cylinder
which forms the body of the young sponge ; they are formed gradually,
not all at once. As the pouches are formed the flagellated cells are
taken up into them, and the dermal cells migrate inwards from the
outside, pressing the flagellated cells asunder, and constitute the
epithelium lining the central cavity of the sponge or "paragaster."
The interspaces between the openings of the horizontal pouches, that
is to say, the niches left between the outer surfaces of these pouches,
constitute the inhalent system of canals. In this sponge the re-
productive cells seem also to be formed from the dermal layer ; in
their undifferentiated form they are full of yolk, and are known as
archaeocytes.

OTHER SPONGES

To Maas (1898) we owe the demonstration that all sponge larvae
are modifications of the type just described. Of the development of
the Hexactinellida nothing is known ; larvae, it is true, have been
observed which seem to originate from unfertilized eggs, and which
resemble the larvae of other siliceous sponges, but their history has
not been followed.

When we turn to the Demospongiae in which the spicules are
arranged in cords, and wrhich constitute the vast majority of sponges,
we can trace a complete series from a development more primi-
tive than that of Grantia to the most modified form, IVgiiming
with Oscarella, which, although devoid of a skeleton, has its all'mities
with the Demospongiae, Maas shows that the embryo is hatched as
an oval blasiula, consisting of a uniform layer of flagellated cells.
During the course of its free life as a larva, the cells of the posterior

44

INVEETEBEATA

CHAP.

half lose their flagella and become granular, so that the blastula is
thus converted into an amphiblastula. The amphiblastula fixes
itself and undergoes a metamorphosis like that of Grantia, but the
resulting sponge, the " Rhagon," is conical not cylindrical, and the

flagellated chambers are pro-
duced as hemispherical pouches
of the inner layer (Fig. 21).

In the development of the
Tetractinellid Plakina, Maas
(1909) describes the larva as
beginning its free life as a
blastula, since the cells constitut-
ing its wall are at first all slender
and ciliated, but the blastocoele
contains a few rounded granular
cells, termed archaeocytes,
which seem to be the mother
cells of the germ cells. The
posterior half becomes granular
by the alteration of the cells,
which lose their cilia, but cells
which are not to be confused
with the archaeocytes are also
budded from this half into the
interior (Fig. 23). Fixation and
metamorphosis occur as usual,
but the resulting sponge has the
form of a shorter cylinder than
is the case with either Grantia
or Oscar ella. By downgrowths
of dermal cells, the interior
flagellated cells become divided
into groups, which, although at
first they retain a portion of the
lumen of the sponge, eventually
become solid; from these solid
masses the spherical flagellated
Fig. 21.— Longitudinal sections through the chambers are formed later (Fig.

free-swimming larva of Oscarella lobularis
in two stages of its development and its
fixation. ( After Maas. ]

A, early larva. B, larva in which posterior cell:-

Finally, in the siliceous
sponge, Esperia (Maas, 1892),

A. early larva. 13. uirva in wiiicn pusieriur I-BIIK ,11 • i -i -i i •

are becoming granular. C, Rhagon shortly after the larva IS hatched RS ail amplll-
tixation. Letters as in two previous figures. blastllla, but the flagellated Cells

cover four-fifths of the surface,

and the granular cells form a solid plug projecting into the interior
of the blastocoele and contain a sheaf of siliceous spicules, ready
for distribution throughout the tissues of the young sponge as soon
as fixation has occurred. Stretching across the blastocoele are

Ill

POEIFEKA

45

Branched cells reminding ns of the mesenchyme cells of the larva
of Grantia.

A

-

^•^S- -o" T^«^- "S."5- ^

Wt-A-

y/

^lllljj,, B

-™^T^:

9

I \Wa

\ -- » r

FIG. 22. — Seven stages in the metamorphosis and fixation of the larva and growth

of the young sponge of Plakina monolopha. (After Maas.)

A, larva in amphiblastula stage ; granular cells budding off cells into interior. B, larva about to
fix itself. C, larva just fixing itself, flagellated half flat. D, fixed larva, flagellated cells beginning to
invaginate. E, " Rhagon " stage. F, G, two stages in subdivision of Rhagon cavity by downgrowth of
septa ; Jt, flagellated cells ; gr, granular cells ; men, " mesencliyme " ; s, septa dividing cavity of Kliagon.

After fixation the flagellated cells collapse to form a solid mass,
which is speedily separated into smaller masses by ingrowths of the

46

INVEKTEBRATA

CHAP.

dermal cells, and these masses become hollowed out to form the
spherical flagellated chambers.

A B

.

mes

arch

FIG. 23. — Two sections of the body-wall of the larva of Plakina monolopha in order to
show the distinction between archaeocytes and mesenchyme. (After Maas. )

A, a piece of wall of erabyro not yet hatched. B, a piece of wall of free larva ; arch, archaeocytes ;

me.«, mesenchyme.

In this series, Grantia forms, not the beginning, but takes the
second place, and, viewing the series as a whole, we see a

progressive shortening of the
Larval life joined to an
anticipation of adult char-
acters. We have, indeed,
before us, typical examples
of the commonest form of
the modification of develop-
mental history from its
primitive form. This consists
in the reflecting back of
structures characteristic of
one period of the life-cycle
to successive earlier periods
in ontogeny. It is called
heterochrony, and its pos-
sible cause will be discussed
in the summary. The merit
of having called attention to
it, and of having emphasised
its importance, belongs to
Lankester.

The development of the
most primitive sponges, the
Asconidae, has been worked
out by Minchiu (1896), and
his results are of great
interest but a little difficult to reconcile with the series determined
by Maas. In the genus Clathrina, the embryo is hatched as an

FIG. 24. — Longitudinal section through the Ainphi-
blastula larva of Espcria luren~i. (After Maas.)

fl, flagellated cells; ijr, granular cells; mes, "mesen-
chyme"; scl, seleroblasts secreting curved spicules ;
syi1, shovel-shaped spiculea ; s/i-, pin-head spicules.

in PORIFERA 47

oval ciliated blastula, with two cells at its posterior pole which are
interpreted as the mother cells of the archaeocytes or primitive ova.
From these cells numerous granular cells are budded off and fill the
interior of the vesicle, but other cells formed by the modification of
individual flagellated cells here and there, which lose their flagella,
also migrate inwards. These latter cells, at fixation, are stated to
burst forth and surround the ciliated cells.

In Leucosolenia, on the other hand, the posterior part of the
interior of the blastula is filled with a mass of granular cells with
small nuclei, and in front of these is a tube of flattened pigmeuted
cells containing a lens-like body. This, according to Minchin, con-
stitutes a rudimentary visual organ ; it disappears at fixation. The
cells of the posterior half of the blastula wall become granular in
situ during the free life of the larva, and so an amphiblastula is
produced. (Fig. 25.)

Further details of these interesting life-histories are urgently
called for. We wisli to know what corresponds to the archaeocyte
in G-rantia. If in this form the archaeocytes are only differentiated
from the dermal cells after fixation, this must surely be a more
primitive arrangement than what obtains in the Asconidae or in the
Tetractinellida, where these primitive ova are differentiated during the
segmentation of the egg. Minchin, indeed (1900), suggests that the
granular cells, which are invaginated whilst the embryo of this sponge
is in 'the tissues of the mother, are archaeocytes and are quite
distinct from the cells forming the one end of the amphiblastula
which he regards as transformed flagellated cells ; but this view
is negatived by Dendy's researches, the results of which have been
described above.

The development of the well-known freshwater sponge Spongilla,
which has been worked out in great detail by Evans (1899), presents
several features of great interest. This sponge belongs to the group
Demospongiae and forms a larva somewhat like that of Esperia,
but the outer flagellate layer extends all round. One end of the
larva is broader than the other and under this end is a cavity. The
rest of the interior is filled with yolk-bearing " archaeocytes," whilst
just under the skin is a layer of flattened cells with dense nuclei,
like those described in the interior of the larva of Grantia. It meta-
morphoses in much the same way as Esperici, i.e. it fixes itself by
the broad end ; but Evans maintains that some of the " flagellate
chambers " are formed at the expense of groups of archaeocytes and
do not owe their origin to the flagellated epithelium which invested
the surface of the larva.

Sponyilla also reproduces itself by buds termed gemmules.
The development of these in the allied genus Ephydatia has been
worked out by Evans (1900). The genimule first appears as a nunil H.T
of wandering cells in the jelly of the sponge, which are distinguished
from their neighbours by possessing deposits of yolk in their cyto-
plasm. These cells gradually collect at a fixed point in the tissues,

48

INVERTEBRATA

CHAP.

which is the centre for the formation of the gemmule. Here they
become massed together so as to form a spherical lump. Other
wandering cells with less yolk follow after them and form a layer

I

cent

FIG. 25.— Longitudinal sections of Amphiblastula larva, just fixed larva, and young
sponge of Leucosolenia variabilis. (After Minclriu.)

A, free-swimming larva. B, just iixed sta-c. C, young sponge four days old ; cent, central cells ;
fl, flagellated cells ; </;-, granular cells ; int, intermediate cells : I, lens ; j,i<j, pigiaeuted cells.

surrounding them, in which the individual cells, as a consequence of
mutual pressure, assume a columnar form. The investment is for a
considerable time not quite complete, and an opening therefore exists.
In this opening are found some specially large cells called tropho-

Ill

POEIFERA

49

cytes, devoid of yolk, but with plentiful dark granules in their cyto-
plasm, which appear to act as carriers of nutriment to the enclosed
yolk cells. The investing cells secrete a membrane on their inner
surfaces. The columnar layer is then invaded by another class of
wandering cells which come from the adjacent tissues of the sponge.
These are clear cells carrying in their interipr peculiar spicules
called amphidiscs. The amphidisc resembles a pair of toothed
wheels joined by an axle. Various stages in the development of
amphidiscs can be seen in the maternal tissues. They first appear
as little needles, similar in shape to the other spicules of the sponge.
The ends of the needles thicken and eventually form wheel-like discs

+ ^*Zrt /s

I • • / <-x ' -v-

1 . ' si x\ i . .' .». •

amph

FIG. 26. — Section through a gemmule-bearing individual of Ephydatia Uembingia.

(After Evans. )

, Amphidisc ; fjenvm, gemmule.

(Fig. 26 ampli). When the amphidiscs have taken up their position
amongst the cells of the investing layer, the cells which carried them
degenerate and disappear.

Before the investment of columnar cells is quite complete, the
trophocytes withdraw from the yolk cells and pass back into
the mother sponge. The inner ends of the columnar cells, after
having secreted the membrane, likewise degenerate and form a sort
of network of fibres between adjacent amphidiscs. The outer portions
of these cells, however, become segregated off from their inner de-
generating portions and pass back into the mother sponge. Before
doing so, however, they secrete on their inner ends another membrane,
which may be called the outer, membrane of the gemmule, since it
unites together the outer ends of the amphidiscs. Where the investing

VOL. I E

50

INVEETEBKATA

CHAP-

layer is finally completed no amphidiscs are found, and this forms
a weak spot through which the inner mass, which is the real hud,
eventually issues forth. The gemmules are set free on the decay of
the parent in the autumn, fall to the bottom of the pool or stream
and remain dormant till the spring. The inner mass then perforates
the weak spot in the membranes, it streams forth in ameoboid

Iroplt

B

<-,i.Tn

•>o,e • . • • ....:

£T.'. I

FIG. 27. — Three stages in the formation of the gemmules of EpliyJutin blembingia.

(After Evans.)

A, investment of columnar cells incomplete, trophoeytes in contact with yolk cells, inner membrane
being formed. B, investment of columnar cells complete ; immigration of scleroblast with amphidiscs.
C, ripe gemmule. Yolk cells form a solid mass; innph, amphidisc ; col, columnar cells; i.m, inner
membrane; o, aperture for escape of embryo; u.m, outer membrane; scl, scleroblast; trojih, tropho-
cyte ; y, yolk cells.

fashion and forms a little mass of cells which develops into a
sponge.

Marshall (1884) has shown that in Spongilla lacustris the
sponges to which the gemmules give rise reproduce themselves by
sexual cells and then perish, whilst the larvae which arise from the
fertilized eggs grow into sponges which produce gemmules ; thus there
is iu this sponge an alternation of generations similar to that with

in PORIFEKA 51

which we shall become familiar when we study the next group,
Coelenterata.

Maas (1906) lias reared the larvae of Calcareous Sponges in
water artificially deprived of all carbonate of lime. The result was
that no calcareous spicules were formed, and when the larva fixed
the flagellated cells formed a solid mass and developed no lumen.
Hence Alaas concludes that the formation of spicules acts as a
stimulus which determines the invagination of these cells to form a
hollow cylinder. This may be true for Grantia, and other Calcareous
Sponges, but it is obviously untrue for Oscarella which has no
spicules.

ANCESTRAL HISTORY

In the introductory chapter it was pointed out that there is
strong evidence that larval forms are, broadly speaking, reminiscent
of ancestral conditions of the stock or phylum. When we find in
the ontogeny of all sponges the blastula form cropping up, and
further find that, in those with the longest larval history this stage
is larval, becoming embryonic only in cases of a short free life, we
feel justified in assuming that it represents in a rough sort of
way the common ancestor of all Porifera.

Such an ancestor — a hollow vesicle of flagellated cells — were it
now living would be termed a colonial Protozoon. In Volvox we
have an organism which, if it did not possess chlorophyll and live
like a plant, would correspond fairly closely to our idea of what this
ancestral sponge must have looked like. Now the great interest
attaching to the blastula is that it appears as a larva in the life-
histories of at least two other primitive groups of Metazoa, and that
as a more or less modified embryo it can be detected in the develop-
ment of all the Metazoau groups. Hence the case for regarding
it as representing the ancestral stock of Metazoa is greatly
strengthened.

But such a stock when it existed must have been of world-wide
distribution, swarming in all the seas and waters of the globe. Such
a world- wide stock would become adapted to different " stations "
and just as at the present day we have bottom-feeding as well as
mid-water fish, so we may imagine that bottom-feeding blastulae were
developed. These, instead of devouring the floating and swimming
organisms like the rest, turned their attention to the microscopic
forms lying on the bottom. Under these circumstances only the
cells on the lower half of the blastula would be effective feeders, and
the more flattened this part became the more effective would be
their work. The other cells would become merely protective and
would tend to lose their flagella, and so the spherical blastula would
be modified into a cap-like form. Fixation would be the next step,
and so far as we can tell from a consideration of the life-histories
of fixed animals belonging to other phyla, fixation is an adaptation
to withstand and at the same time take advantage of currents. The

52 INVEKTEBRATA CHAP, in

larva, instead of creeping about seeking fresli food, holds 011 with its
protective cells and lets the current waft fresh food into its reach.

So far our reasoning appears safe. But the porocytes baffle
explanation ; we cannot picture to ourselves a process by which cells
converted themselves into drain-pipes, when we remember that
every step in the process must have been functional and must have
had a survival value. We can only imagine that the hollowing out
of a cell is perhaps a shortened reminiscence of the process by which
gaps in the attached rim, which must have existed to allow the
ingress of water, became surrounded by protoplasm. The need for
extending the surface of absorption, once fixation were accomplished,
would account for the extension of the area of flagellated cells by
their invagination, so that collectively they took on the form of a
cylinder ; but the formation of the osculum is utterly obscure.

In some few cases we can compare ancestral history as recorded
by fossils, with ancestral history deduced from embryology ; we can
then see, as compared with the record deduced from fossils, what an
abbreviated sketch is constituted by the embryological record. In
the present case it is true we have no fossils to guide us, but the
abbreviation of ancestral history, as reflected in larval history, must
be intense. The later stages of the history of the race, the gradual
complication of the chamber system, is mirrored in the post- larval
development : the first fixed Grantia is at first an Ascon, and only
gradually takes on the Sycon characters as it grows in size.

The history of all sponges just after fixation would be a most
interesting field for research, and would throw much light on their
mutual affinities.

LITERATURE REFERRED TO

Dendy, A. On the P.seudo-gastrula Stage in the development of Calcareous Sponges.
Proc. Roy. Soo. Victoria (Australia), 1898.

Evans, R. The Structure and Metamorphoses of the Larva of Spongilla lacustris.
Quart. Journ. Mic. Sci., vol. 42, 1899.

Evans, R. A description of Ephydatia blembingia, with an account of the formation
and structure of the gemmule. Quart. Journ. Micr. Sci., vol. 44, 1900.

Maas, 0. Zur Metamorphose der Espcria lorenzi. Mitt, aus der Zool. Station zu
Neapel, vol. 10, 1892.

Maas, 0. Die Keimblatter der Spongien und die Metamorphose von Oscardla
(Halisarca). Zeit. fur wiss. Zool., vol. 63, 1898.

Maas, 0. Die Weiterentwicklung der Syconen nach der Metamorphose. Zeit. fur
wiss. Zool., vol. 67, 1900.

Maas, 0. Uber die Einwirkung carbonatfreier und kalkfreier Salzlb'sumgen auf
erwachsene Kalkschwamme und auf Entwicklungsstadien derselben. Arch. f. Ent-
wick., vol. 27, 1906.

Maas, O. Zur Entwicklung der Tetractinelliden. Verb, der Deutschen Zool.

Gesell., 1909.

Marshall, W. The reproduction of Spongilla lacustris. Sitzungsber. Naturforsch.

Gesell. Leipzig, 1884.

Minchin, E. Note on the Larva and the Post-larval Development of Leucosolenia
variaMlis, with Remarks on the Development of other Asconidae. Proc. Roy. Soo., vol.

60, 1896.

Minchin, E. The Porifera. Lankester's Treatise on Zoology, vol. iii., 1900.

Schulze, F. E. Untersuchungen iiber den Bau uud die Entwicklung der Spongien
I. Mitt, liber den Bau und die Entwicklung von Sycandra raphanus. Zeit. fur
wiss. Zool., vol. 25, Suppl. 1875.

CHAPTER IV

COELENTEEATA

Classification adopted —

Hydrozoa

Scyphozoa

Actinozoa

Hydrida

Hydromedusae..

Narcomedusae

Trachymedusae

Siphonophora

fAlcyonaria
IZoantharia

I G-ymnoblastea
\Calyptoblastea

Edwardsiae
Hexactiniae
Cereanthidae
Zoanthidae

Ctenophora

Cydippidea

Lobata

Cestidea

Platyctenea

Beroidea

THE Coelenterata are considered by many zoologists to be closely
related to the parent group from which the other groups of Metazoa
have sprung. In simplicity of general organisation they rival the
Porifera, since the bodies of the adult Coelenterates, like those of
Porifera, are composed of two layers of cells with an intervening jelly.
Ever since in 1859, Huxley compared these two layers in a Coelen-
terate to the two primary layers of the Vertebrate embryo, they
have been termed ectoderm and endoderm.

The most interesting thing about the relationship between the
Porifera and the Coelenterata is that whilst the earliest stages of
development in the most primitive representatives of each group
are strikingly similar, and whilst in both cases a two-layered adult
condition is reached, yet the steps by which this goal is attained
differ so totally in the two cases that the two layers cannot be
regarded as corresponding to one another in the two groups.

53

54 INVEETEBRATA CHAP.

I. HYDEOZOA

TUBULARIA

The type which we select for special descriptions is the common
hydroid Tubularia, species of which are abundant in shallower water
on British, Mediterranean, and American coasts. We base our
account on the careful work of Brauer (1891) who has worked out the
development of the Mediterranean species of Tubularia mesembryan-
themum.

The British Tubularia indivisa is found attached to the bottoms
of old boats. The medusa in most species of this genus remains
permanently attached and the young pass through the earliest stages
of their development within the bell of the mother. In this respect,
as in the permanent attachment of the medusae, Tubularia is far
from exhibiting primitive or typical conditions, but the free-
swimming medusae of any particular species cannot always be
obtained, and the eggs of these can often only be reared through the
earlier stages of development. In many cases the hydroid stage is
unknown, and a picture of the complete development of a typical
hydroid which produces free-swimming medusae, can only be made
out by piecing together the only fragments of the life-histories of
many species which are known. It is for this reason that, in spite
of its manifest disadvantages, we choose Tubularia as a type.

The egg and early segmentation stages are found by examining
transverse sections of the gonophores and by means of whole
mounts. The gouophores are the rudimentary medusae which remain
attached to the colony throughout life. On the mauubria of these
the eggs and sperm are produced. The eggs are dehisced into the
bell, in wThich they undergo practically the whole of their develop-
ment, so that the bell is no longer a locomotor organ but a nursery.
The eggs are amoeboid and appear to segment fairly regularly,
but they are deformed by mutual pressure in the confined space in
which they find themselves. Only two or three are dehisced at one
time.

The segmentation of the egg is somewhat irregular and leads,
after about sixteen segments have been formed, to the formation of a
hollow' vesicle or blastula. It is, however, a remarkable circumstance
that what appears to be an abnormal form of segmentation frecp^ently
occurs and leads also to the formation of a regular blastula. In this
latter form of development the nucleus divides repeatedly before any
division of the protoplasm occurs, and then subsequently the multi-
nucleate mass is cut into cells. When we find that these two methods
of development sometimes characterize different genera of the same
class of the animal kingdom, we are apt to think of them as very
different, but their occurrence side by side in the same species shows
that the physiological difference separating them must be very slight.

The blastula stage is succeeded by a solid morula stage. This

IV

COELENTEKATA

55

word, which literally means "mulberry," is used to characterize a
condition where the cells which constitute the embryo form a com-
pact spherical mass. The morula stage is reached by the proliferation
of cells from the walls of the blastula in sufficient number to fill up
the interior. Whether these cells are budded from all parts of the
blastula wall or only from a certain area of it, has not been made out.
In the case of the eggs of the free-swimming medusae, however, it
is beyond all question that these cells are budded only from one end
of the blastula, and none of Brauer's figures are inconsistent with

FIG. 28.— Two methods of
formation of the blastula
in Tubularia mesem-
bryanthemum. (After
Brauer. )

A, egg segmenting in normal
method. B, egg segmenting
in abnormal method.

coe

inst

FIG. 29. — Formation of endoderm in Tiifm/'/ri'/
mesembryanthemum. (After Brauer. )

A, budding of endoderm cells from blastula wall.
B, morula stage, coe, spaces which will ultimately
form the coelenteron ; ed, ectoderm ; vn/l, endoderm ;
inst, interstitial cells.

the assumption that this is the case with the blastulae of Tubularia
also. In any case a solid morula stage is soon reached in which the
whole interior of the blastula becomes clogged up with a mass of cells.
This mass of cells constitutes the rudiment of the endoderm of the
adult, whilst the original blastula wall forms the ectoderm. In the
.solid mass of endoderm spaces begin to appear owing to the absorp-
tion of some of the central cells. These spaces (coe, Fig. 29)
eventually coalesce so as to form one cavity which is the gastral
cavity or coelenteron of the adult. The embryo has now the form of
a circular disc, and from its edges a series of blunt protuberances
grow out. These are the rudiments of the aboral tentacles of the
adult : they are bent towards the future aboral end of the body. At

56

INVERTEBRATA

CHAP.

the opposite or oral end is a spot where ectoderm and endoderm thin out,
and there eventually the mouth will be formed by a perforation of both
layers. The disc-shaped embryo grows rapidly in the direction of its

FIG. 30. — Section of embryo of Tubularia mesembryantliemum showing the formation
of the aboral tentacles. (After Brauer.)

ali.t, aboral tentacle ; coe, coelenteron ; o, spot where the mouth will be formed.

principal axis and becomes cylindrical, and finally develops round its
oral end a series of small protuberances which are the rudiments of
the oral tentacles of the adult. By this time the mouth has been
formed and the aboral tentacles have become long and slender
(Fig. 31).

A

D

Fi«. 31. — Five views of external features of different stages in the development of the
embryo of Tulularia indivisa. (After Allman. )

A, oval embryo. B, aboral concavity appears. C, rudiments of aboral tentacles. D, tentacles long ;
embryo becomes cylindrical. E, oral tentacles formed, (ib.t, aboral tentacles ; o.t, oral tentacles.

The embryo is now called an Actinula, and is ready to leave the
bell of the gonophore. It escapes from its nursery, and creeps about
on the bottom of the sea with its mouth turned downwards, but
finally it attaches itself by the aboral end. It then rapidly grows
in height, and from its sides daughter persons are budded, so that
it forms an upright shoot in the adult colony. From its base arise

IV

COELENTERATA

emb

B

creeping stolons which give rise at intervals to other upright shoots.
Its lower part secretes a horny shell, the perisarc.

The adult colony,
however, is still unripe
sexually ; full sexual ma-
turity is only reached by
thegonophores produced
subsequently, and thus
we have an alternation
of asexual and sexual
generations.

The development of
these gonophores in
the case of Tubularia
(as well as in the case of
many other genera) has
been worked out by
Gotte (1907) ; we follow
his account in what
follows. From just above
the region of the aboral
tentacles, finger-like
stolons grow out, and on

A, gonophore with discoid embryo ; opening of umbrella-cavity
just formed ; radial canals clear. B, gonophore with actinula
larva just escaping ; radial canals have disappeared. Act, actinula ;
emb, embryo; r.c, radial canal; sp, manubrium or spadix ; ?i,
opening of umbrella-cavity.

•at.

Act

FIG. 32. — Two gonophores of Tubularia indivisa with
developing embryos inside. (After Allman.)

these, lateral protrusions
arise, which are the
medusa -buds. At the
tip of such a bud, the

FIG. 33. — Stages in development of Actinula larva of Tubularia indivisa. (After Allman.)
A, creeping larva. B, first fixed form, ab.t, aboral tentacles ; o.t, oral tentacles ; y/cc, perisarc ;

si, stolon.

ectoderm thickens to form a mass of cells, and in this mass a cavity
develops, the future umbrella-cavity.

58

INVEETEBEATA

CHAP.

The mass is termed by German authors " Glockenkern," which
we may translate " bell-rudiment " ; it is crescentic in section with
its concavity directed downwards. Into this concavity fits a pro-
trusion of the endoderm of the medusa-bud ; this is the " spadix,"
the rudiment of the future mauubrium, so far as its endodermal portion
is concerned. From the base of the spadix four hollow protrusions

of endoderm grow out as canals, and
insinuate themselves between the ecto-
derm of the bud and the outer ectoderm
of the bell-rudiment. The spots where
these canals bud out are the interspaces
between four vertical, solid ridges of
endoderm called the taeniolae, which
project into the gastric cavity of the
spadix.

The canals are termed the radial
canals, and they eventually push out
short protrusions of the ectoderm which
are the rudiments of the medusa
tentacles. The radial canals flatten
out and become fringed with flat
extensions of endoderm. These exten-
sions meet one another in the centre
of the interradii, and so constitute
continuous sheets of endoderm covering
the interradii and forming the so-called
endoderm lamella (Fig. 35, en.l}.

The apex of the medusa-bud consists
only of the ectoderm of the bud and
the outer ectoderm of the bell-rudiment
through developing medusa-bud cioseiy pressed together. Absorption

ot lubidana mesembriianthemwn. n ,n T y i

(After Gutte.) °* these adpressed layers now takes

PlaC6> and an Opening is thus formed

which places the cavity ot the bell in
connection with the exterior, and
through this aperture the manubrium
often protrudes. The thin ectoderm
round the edge of the aperture forms
the velum. In Tubularia the hollow
radial canals are transitory structures, and their lumina soon become
crossed by cords of cells.

The genital cells are found in the ectoderm covering the lower
part of the spadix. According to Brauer (1891) they originate as
interstitial cells of the ectoderm in the early stages of development
of the medusa-bud ; they then migrate through the jelly into the
endoderm, and finally iuto the ectoderm covering the spadix
(Fig. 36).

FIG. 34. — Three longitudinal sections

In A, the youngest, the bell-rudiment
is just formed. In B, the spadix and
radial canals are differentiated. In C, the
umbrella-cavity is open to the exterior.
<//.•, bell-rudiment (Glockenkern); </•'''''>
genital ectoderm ; r.c, radial canal ; up,
spadix ; t, taeniola ; u, umbrella-cavity ;
v, velum.

IV

COELENTEKATA

59

cn.l. re

ym ec,

FIG. 35. — Four transverse sections through the developing gonophore of
Tiibularia mesembrycoit/iemuin. (After Gotte.)

A, section through base of gonophore showing the four
taeniolae ; t, taeniola. B, section through upper part of older
^"^'"-^S^^^K! , ,/- gonophore ; r.c, radial canal ; r'c', spot where two radial canals
r "Zwfe—caiw'Np'X c' ' ' ' join; sp, spadix ; u, spaces, portions of the irregular umbrella-
cavity. C, section through still older gonophore ; letters as
before; en. I, so-called endoderm lamella. D, section through
almost mature gonophore. r.c, remnants of cavity of radial
canals ; gen.ect, generative ectoderm clothing the spadix.

FKEE MEDUSAE

When we contrast with this develop-
ment the life-history of the free medusae
so far as it is known, we find many marked
differences. Our principal source of in-
formation on this subject is Metschuikoff
(1886), who captured the free medusae of
Tiara, Ratlikea, Oceania, Clytia, etc., and
kept them in aquaria till they had de-
posited their eggs. He was then able to
rear the embryos through the larval stages,
until they produced young hydroid colonies.

In nearly every case he found that the
egg underwent a very regular segmentation
which led to the formation of a blastula ;
this was at first spherical but soon became

FIG. 36. — -Longitudinal section
through very young gono-
phore-lnid of Tnlnilm-ia mes-
embryanthemum to show the
origin of the genital cells.
(After Brauer. )
Letters as in Fig. 34. In addi-
tion : (/oil, genital cells originating
in ectoderm ; ijen~, genital cells which
have penetrated into endoderm.

60

INVERTEBKATA

CHAP.

oval and ciliated, with an anterior broad and a posterior more pointed
end, and which swam freely about in the water. At the pointed

FIG. 37. — Four stages in the development of the planula of Clytiu. (After Metschiiikoff. )

A, blastula stage. B, formation of endoderm by immigration of cells of blastula wall at one pole.
C, endoderm, a solid mass, half-tilling the cavity of the blastula. D, free-swimming planula larva.
end, endoderm.

end, and at this end alone, cells migrated inwards and formed a mass
which rapidly increased in extent, owing, not only to the successive

immigration of new cells, but
also to the division of the im-
migrated cells in situ ; and so
the blastula was converted into
what is termed a planula.

In the vast majority of
Hydrozoa, and also in many
Actinozoa, the organism enters
on its free life in the " planula "
stage. A planula is an oval
larva covered with a layer of
ciliated cells containing a solid
mass of cells inside. Develop-
ment within the bell of the
parent medusa till the adult
form is attained, such as occurs
in Tubularia, is exceptional.
Hence the planula is termed

FIG. 38.-Three stages in growth of fixed planula tllG typical larva of the Coeleil-

of ciytia. (After Metschnikoff. ) terata. This planula, after a

short free life, attaches itself
to the bottom by the broad
end, which flattens out. Then,
and then only, absorption of the

central cells takes place, and a gastric cavity makes its appearance.

The broad end becomes divided by indentations into lobes, each of

A, at moment of fixation. B, a short time after.
C, a day after, st, divisions of broad attached end
which are the rudiments of stolons.

IV

COELENTEEATA 61

which constitutes one of the creeping stolons. The narrow end
grows up and develops into the first polyp, the mouth and tentacles
being formed as described in Tubularia. Metschnikoff's results
have been confirmed in the most gratifying manner by Eittenhouse
(1910), who studied the development of the eggs of the medusa
Stomotoca apicata. The sole point in which he is inclined to differ
from Metschnikoff is, that he regards the endoderm as arising by the
budding of cells from the cells constituting the blastula wall, rather
than from the migration of cells forming part of that wall into the
interior. Thus we see that processes, winch in the case of Tubularia
are completed before the larva leaves the bell of the mother, do
not occur in the case of the free medusae till long after the larva
is fixed.

FIG. 39. — A young colony of Glytia reared from a plauula in the aquarium.

(After Metschnikoff. )

U, blastostyle ; g, rudiment of medusa ; per, perisarc.

A thorough study of the development of the medusae and gono-
phores has been made by Gotte (1907). In the series of progressive
modifications of development which can be constructed from the
development of the forms which he describes, Tubularia and
Pennaria (in which the medusae occasionally become free) take the
second place. The most primitive type of development is found in
forms like Podocoryne, in which the medusa regularly becomes a
free-swimming organism, and swims about for a long time, and eats
and grows before it develops genital cells.

In Podocoryne, after the medusa-bud has attained the stage just
described for Tubularia,, after the radial canals have been formed,
they give rise to lateral outgrowths which meet those of adjacent
radial canals, and in this way a circular canal is formed ; then the
freely-projecting ends of the radial canals give rise to free tentacles. •
By the formation of flat solid extensions from the lateral walls of
the radial canals, which meet each other, a continuous sheet of
endoderm is formed which spreads over the whole extent of the bell.
This is called the endoderm lamella. The manubrium attains a

62

INVERTEBRATA

CHAP.

B

'.C

mouth, and the whole medusa becomes free by the absorption of
the stalk of the bud. Generative cells are only matured after
a considerable period of free-swimming life.

On the other hand, accord-
ing to Gotte, in Clava the bell-
rudiment is formed but the
umbrella-cavity never opens to
the exterior, nor are there any
radial canals formed, and the
whole bell-rudiment is absorbed
before the germ cells are shed.
In such forms as Clava the
generative cells of at least one
sex — in the case of Clava of
both sexes — can be detected
in the stalk of the person
(blastostyle) which bears the
gonophores. Their develop-
ment in this genus has been
described by Harm (1903).
They appear to arise from
amongst the interstitial cells
of the ectoderm, but, as is also
the case with the genital cells
of Tubularia, they migrate
early into the endoderm, where
they grow. They reach the
spadix when fully ripe, and
burst through the ectoderm
there (Fig. 42).

In Cord'i/lophora the bell-
rudiment remains a solid mass
of cells, part of which is
converted into generative
cells.

In Sertularia the gono-
phore is a broad-based lateral
swelling on the blastostyle,
the bell-rudiment separates
from the ectoderm and splits

ten

-v

sp

Fin. 40. — Two longitudinal sections through the
developing rnedusa-bud of Podocor/jm- curneii.
(After Gotte.)

A, before umbrella-cavity is open to the exterior. imperfectly, the Vestigial 11111-

B, after umbrella -cavity is open to the exterior. brella-CaVlty beinff CrOSSed by

o.r, circular canal ; gen, developing genital cells ; r.c, 11 f 1 1 ' 1 £ ll

radial canal ; sj>, (in A) cavity of the spu.lix, (in B) wall tratieCUlae ; aUCl filially, in

of the spadix; tun, tentacle ; u, umbrella-cavity. HaleClUlll 110 bell-rudillient at

all is formed.
The last two forms belong to that division of Hydromedusae

O i/

termed Calyptoblastea, which possess hydrothecae, and in which the
mouthless person, or blastostyle, which bears the gonophores, is

IV

COELENTERATA

63

enclosed in a special case, the gonangium. This gonangium is
secreted by a special outer layer of ectoderm, the mantle layer,
which breaks away from the inner ectoderm covering the medusa-
bud. In Hctlccium a set of endoderm tubes, like the radial canals,
grow out from the blastostyle and ramify in the mantle.

Gotte interprets the series of forms which he describes, as steps
in the building up of the medusa out of what was originally nothing
but a lateral swelling on a hydroid person (as the member of a Coelen-

c.c

u

FIG. 41. — Four transverse sections through the developing medusa of Podocoryne
to show formation of circular canal and endoderm lamella. (After Gotte.)

A, through base of young gonophore showing four taeniolae. B, through older bud showing four
separate radial canals. C, through base of older bud showing the fringes growing out from the radial
canals which form the endoderm lamella. D, through upper part of older bud showing circular canal.
In this figure the roof of the umbrella-cavity is grazed. Letters as in previous figure ; en.l, endoderm
; (, taeniola.

terate colony is termed). This swelling is caused by the genital
cells, and is therefore similar to the swelling produced by the
ovary or testis of Hydra. The majority of zoologists, however, read
the series in the opposite direction and, as it seems to us, with
infinitely more justice. They regard the " gonophores " as degenerate
forms of medusae, which once were perfectly developed and became
free, but have ceased to be detached, and so the structures which a
free medusa uses for swimming have become functionless in them.
H"ow else can the umbrella-cavity of Clava, which never opens and
becomes completely resorbecl, be interpreted 1

64

INVERTEBRATA

CHAP.

A

u

At the same time Gotte's results have thrown light on how
a medusa was developed out of a hydroid form. It used to be
held that a medusa was essentially a hydroid shortened in the
direction of the mouth-foot axis. This shortening, it was thought,

had caused the oral and aboral walls of
the peripheral portions of the stomach
of the hydroid to adhere to one another,
and so to form a solid plate of endoderm,
the so-called endoderm lamella; thus
leaving the lumen only in the centre, in
the extreme outer edge (the circular
canal), and in four radiating lines (the
radial canals).

But if we follow Gotte we must
imagine a simpler process of evolution.
The bell of a medusa is, according to him,
merely a web connecting the basal parts
of the tentacles of a hydroid, and a
medusa is related to a hydroid as a duck's
foot is related to a hen's foot.

We may suppose, then, that originally
the hydroid persons were separated from
the mother, and crept about, as still
happens in the case of the buds of Hydra,
and that these persons eventually de-
veloped genital organs ; but that a
differentiation in these buds took place,
so that some never separated, but
remained permanently immature and
asexual, whilst those that did separate
FIG. 42.— TWO longitudinal sec- developed a swimming web. In this way
tious through the developing t]ie alternation of generations so char-

Eronophore or Clara squamata. , • ,• P TT i T

(After Harm.) acteristic ot Hydrozoa was developed.

A, young gonophore with rudi-
mentary umbrella-cavity and unripe SIPHONOPHOPA
ovum embedded in endoderm. B, fully
developed gonophore with ripe ovum. rrii Q,',O , 1, n i-

o,, ovum; I, umbrella-cavity. . The Siphonophora are floating or

swimming Hydromedusae. The most

ingenious and plausible hypothesis as to their origin is that put
forward by Korschelt and Heider (1890;, who regard as most
primitive those forms like Physalia and Velella, which float only,
and are without those engines of propulsion known as nectocalyces.
Korschelt and Heider (1890) suppose such forms to have been
derived from larvae of ordinary Hydromedusae, which have fixed
themselves to the surface film of the water.

That this is a possible and even probable contingency will lie
self-evident to any one who has watched young starfish walking
upside down on the surface film, like flies on the ceiling of a room,

IV

COELENTEKATA

65

or who has seen some members of a swarm of Ascidian tadpoles thus
fix themselves to the film. The surface film, although able to sustain
the weight of a larva, would soon bend under the growing weight of
the hydroid colony which developed from it, and this would lead to
a cupping of the base. If we suppose this base to secrete mucus and
to entangle bubbles of air, the elements of a float would thus be
presented.

FIG. 43. — Three stages in the development of a Siplionophore (CystaUn inn,i,,iinstrica).

(After Haeckel.)

A, planula with Boat, an open inva^iuation of the aboral ectoderm. B, Older larva, a single
tentacle formed. C, still older larva in whirh the definitive endoderm is formed, ami in \vhk-h
buds of other persons have been formed, b, buds ; end, endoderm ; jjn., float ; ten, tentacle.

The earlier stages in the development of these Siphonophora
have not been made out, but the planula larva is well known. The
peculiarity of this larva lies in the fact that the large vacuolabed
internal cells which occupy its interior, are not directly converted
into the endoderm of the adult, but that they bud off smaller cells
on their outer sides, which form the definitive endoderm which
persists throughout life.

As in other planulae, the narrow end lengthens and becomes

VOL. I F

66 INVERTEBKATA CHAP.

converted into the body of the first hydroid polyp, at the apex of
which the mouth is formed ; but the broad end develops an ectodermic
invagination, the rudiment of the float, at the spot where the
attached base would naturally be looked for if we were dealing with
planulae of Hydromedusae. A single tentacle sprouts from the base
of the polyp, and above this, i.e. nearer the float, is a growing1 zone,
from which other polyps arise.

In many Siphonophora certain of the medusoid buds lose their
genital cells, and even the manubrium, and become organs of
locomotion merely. These organs arise in the part of the growing
zone nearest the float, morphologically the most basal part. In one
group the adult relies on these modified medusae (nectocalyces)
alone for swimming, the float having disappeared ; and in such cases,
which we regard as the most modified of all, the endoderni cells in
the base of the planula secrete oil drops, and the first definite organ
to be formed in this region is a huge nectocalyx.

To this theory of Korschelt and Heider there are opposed two
other theories, viz. the medusome theory of Haeckel (1888) and the
theory of Chun (1887).

According to Haeckel, the whole Siphonophore colony is merely
a medusa which budded, as some few medusae are known to do.
Every person is supposed to be a modified medusa ; the bells of the
medusae are supposed to be represented by the translucent leaf-like
bracts, termed hydrophyllia, which many species possess ; and the
hydroid-like persons are their " manubria," which are supposed to
have migrated out from them through a slit in the bell. The violent
dislocations required by this theory belong to the period of imagina-
tive morphology.

Chun agrees with Korschelt and Heider in regarding the
Siphonophore as a Hydromedusan colony, containing both hydroid
and medusoid persons ; but he regards the float as a modified medusa,
in which air has replaced water. It is, however, very difficult, if
not impossible, to picture a series of ancestors in which one of the
medusa bells gradually replaced its contained water by air. In other
words, Chun's hypothesis transgresses the law of functional con-
tinuity, which should be exemplified in any supposed phylogenetic

change.

NARCOMEDUSAE AND TRACHYMEDUSAE

The Narcomedusae and Trachymedusae are usually stated to be
Hydromedusae, in which the egg develops directly into a medusa
without an intervening hydroid stage. A more correct statement
of the case would seem to be that the egg develops into a modified
hydroid person, which does not bud, but which, by the forma-
tion of a web, becomes directly transformed into a medusa.
The fact that both these groups are pelagic in their habit has
rendered the formation of a fixed budding colony of hydroids
impossible. Therefore the development is hurried on, and the first

IV

COELENTEI1ATA

person develops into a medusoid, passing, in some cases at least,
through a hydroid stage in the course of its development.

In the development of Geryonidae, a family of the Trachy-
medusae, it is usually stated that a spherical blastula is at first
formed, and then that the inner vesicular
portion of each cell of the blastula becomes
detached from the outer end, and that these
inner portions unite to form an endodermic
vesicle. In this way, it is said, the two-
layered condition is reached.

This view is founded exclusively on
views of living segmenting eggs which,
owing to their spherical character, could not

be orientated; and on the assumption that FIG. 44.— EmbryoofaGeryonid
this mode of the formation of endoderm
and ectoderm actually occurs, it has been
regarded as typical delamination, and as
representing the primitive way in which a
two-layered condition was arrived at.

Strong objections may be urged against this view. The
development of the Trachymedusae and Narcomedusae is greatly
modified as compared with that of the more normal Hydromedusae,
on account of their mode of life ; and further, when we consider
how easily mistakes can be made as to the nature of a process, unless
carefully orientated embryos are examined and cut into sections, we
must regard it as very questionable whether the kind of delamination
described in the Geryonidae does actually take place. It is possible
that in this family we have to do with a proliferation of the cells
forming the blastula wall, at one side of the blastula, but that the
area of proliferation is of considerably greater extent, relatively to
the whole surface of the blastula, than it is in the case of the blastulae
of ordinary Hydromedusae. If this pole were turned towards the
observer, he would receive the impression that he was looking at a
sphere, from the whole of whose circumference cells were being budded
inwards.

( Carmarina fungiformis) in
which endoilerm cells are
being budded oil'. (After
Metschnikoff.)

en//, enclodenn.

II. SGYPHOZOA

AURELIA

If we now turn our attention to the great group of the Scypho/u;i,
we find that the development of the genus Aurelia has been fully
worked out, the latest accounts being given by Hem (1!)00) and
Friedemann (1902). These workers used a mixture of 100 parts
concentrated solution of corrosive sublimate, with 2% acetic acid, to
[•reserve the larvae of Aurelia.

This common jelly-fish swarms on both sides of the Atlantic.
As in all Scyphozoa the genital cells are produced from the endoderm

68

INVERTEBEATA

CHAP.

777

FIG. -45. — Early stages in the development of Aureliu
aurita. (After Hein.)

A, blastula stage. B, gastrula stage, lift, blastopore ; m, cells
budded from the blastula wall which migrate into the interior
and disintegrate.

of the stomach, and are discharged into its cavity, — where they are
fertilized by spermatozoa of other individuals taken in with sea-
water. The fertilized eggs escape from the mouth but are retained
for a considerable period in pockets of the inner surface of the oral arms.

These pockets can be

B recognized in the sur-

face view as opaque
spots. If they are
slit open by needles
under sea water the
embryos can be ex-
tracted.

The embryos can
be preserved in cor-
rosive sublimate and
acetic acid, or in
osmium acid, and
mounted whole ; or
else embedded in
celloidin, orientated,
and cut into sections

parallel to their longitudinal axis. When such sections are examined
it is found that the egg segments with great regularity, and that
a spherical hollow blastula is formed. The cells forming the outer
wall of this blastula bud off other cells which migrate into the
interior, and it looks
as if we were about A
to witness the forma-
tion of a solid planula ;
but the cells wliich
thus migrate inwards
break up into granules
and are absorbed, thus
serving as food for the
rest. Then, at one
end, the cells forming
the wall of the blastula
are invaginated, and
in this way the single- Aurdia aiirita' (After Hein')

layered blastula is COn- A, free-swimming planula. B, stage just after fixation, li/i, blasto-
pore reduced to a mere slit, nem, nematocysts.

verted into a hollow,

double -layered structure termed a gastrula. The opening of the
invagination is termed the blastopore. The conversion of a blastula
into a gastrula is called the process of gastrulation.

The blastopore never closes and eventually forms the mouth,
although it becomes contracted to the finest capillary dimensions.
The yolk granules in the cells become absorbed, and the spherical
gastrula becomes converted into an oval one, with a broad basal end

netn

FIG. 46. — The fixation of the free-swimming larva of

IV

COELENTERATA

09

and a more pointed end where the mouth opens. Thus by a single
process a stage is reached which, in the Hydromedusae, is aUa.inc.l
first by a process of the immigration of cells, then by the absorption
of the more central cells, and lastly by the formation of an aperture
to the exterior.

The embryo now emerges from the maternal pockets and swims
freely about by means of its cilia. The outer cells commence to show
traces of the formation of nematocysts, whilst the inner cells develop
large vacuoles, as in Hydra. It appears that, as in the blastula stage
so also in the gastrula stage, cells migrate from the wall of the
stomach into its cavity and are digested.

After swimming about for four or five days the larva? attach
themselves by their broad ends, the ectoderm cells of which secrete an

o.c

FIG. 47. — Two longitudinal sections through two Hydra-tiibae of different a-vs.
A (after Hein), through a specimen with four tentacles. The section gees through the origin of
a tentacle. B (after Friedemann), through a specimen witli eight tentacles, showing the stomach
pocket intervening between two taeniolae. o.c, oral cone; s.p, stomach pocket; t, tentacle; t.l>.
tentacle bases of vacuolatod endoderm.

•

adhesive secretion. The attached larva becomes gradually some-
what flattened, and passes from a cylindrical to a cup shape. The
endoderm cells in the neighbourhood of the mouth multiply rapidly to
form a slight elevation or oral cone. The ectoderm cells in tins
region do not multiply but become stretched so as to form a thin
flattened layer. The almost obliterated blastopore becomes now
widened so as to form the permanent mouth ; it becomes indeed quite
a gaping opening.

Immediately after this, four primary tentacles arise ;is w;irts •
surrounding the mouth. The interior of each is occupied by a solid
cord of endoderm, and the ectoderm covering it becomes crowded
with nematocysts. Alternating with these tentacles there arise four
taeniolae or ridges of the endoderm projecting into the stomacb

70

INVEETEBEATA

CHAP.

cavity. Each of these is produced hy an inwardly-directed fold of
the endoderm, between the limbs of which is jelly. These taeniolae
are also termed septa (Fig. 48).

Then a circular depression appears in the ectoderm on the upper
part of the larva, which marks off the oral cone from the bases of the
tentacles, and just above the upper ends of the four endodermal folds
this depression appears to be deeper. From the bottom of these
deeper depressions, which are termed the septal funnels, ectoderm

cells are budded off and force
their way into the jelly between
the limbs of the taeniolar folds.
These cells develop fine mus-
cular fibrils on their external
surfaces, which form the four
longitudinal septal muscles.
These muscles extend down
to the base of the larva ; they
are exceedingly irritable and
serve to contract it (Fig. 49).

The larva which is now
provided with a flattened upper
surface or oral disc, with four
long tentacles with solid axes,
with four endodermal septa,
and four ectodermal septal
muscles, is termed a Hydra-
tuba or Scyphistoma. Four
secondary tentacles alternating
with the first four are soon
added, and eventually eight
tertiary ones, alternating with

,-< i j

the PrmiaiT and secondary, so
that in all sixteen are formed.

A, grazing the upper surface or oral disc. B,
through the middle of the body, s.p, stomach pocket ;

't taen?oeC. CeUs ^'"^ "'" ^ °'' "

FIG. 48. — Two transverse sections through a
Hydra -tuba witli four tentacles. (After
Hein.)

As Sir J. Duly ell (1847),
the first discoverer of this larva
showed, lateral buds like those
of a true Hydra can be formed,
which repeat the structure of the parent and eventually become
detached, and stolons can grow out from the body wall just above
the base, extending a short distance, and from them other hydra-
tubae can be given off.

Friedemaun (1902) takes up his account of the development
where Hein left off. The eight -tentacled hydra-tuba grows in
size as it captures more and more prey. Then eight new
tentacles make their appearance alternating with the former, so
that the animal now possesses sixteen tentacles. The number is
then raised to twenty-four by the appearance of eight new ones,
and with this number the hydra -tuba attains the maximum of

IV

COELENTEEATA

71

its development. The nematocysts on the tentacles increase till,
by their aggregation, they form warts and finally garland-like
thickenings.

Meanwhile, whilst the number of tentacles is increasing from
sixteen to twenty-four, other changes supervene. Four new and
larger invaginatious of the ectoderm of the oral disc make their
appearance, just in the positions occupied by the old septal funnels.
These are the rudiments of the four sub-genital pits of the adidt.
Just under the oral disc a hole, the ostium, appears in each taeniola,
so that this structure is transformed from a complete ridge into a
pillar, and the four gastric pouches of the hydra-tuba become in
this way converted into the so-called ring-sinus (Fig. 51).

The free edge of the taeniola thickens and grows out into two

FIG. 49. — A, a Hydra-tuba with eight tentacles.
(After Friedemami.) B, longitudinal section of
a part of a similar specimen to show origin of
septal funnels. (After Hein. )

s.f, septal funnel ; s.musc, septal muscles; st, incipient
stolon ; ten, tentacle ; t, taeniola.

FIG. 50.— Oral view of Hydra-
tuba with twenty tentacles.
(The tentacles are repre-
sented as cut off. ) (After
Friedemaim. )

sp, stomach pouch ; t, taeniola.

diverging lips, which are the first rudiments of the gastral filaments,
and these are covered in the adult with specially active digestive
cells. From the oral side of the first eight tentacles there appear
eight bud-like warts on the oral disc, which are the rudiments of the
sense-organs of the adult. Beyond the ring-sinus eight lobes grow
out ; four of these, termed per-radial, are outpouchings of the original
spaces between the taeniolae, whilst the other four, termed inter-radial,
take their origin from those portions of the ring-sinus which have
developed from the perforations in the taeniolae. Thus the oral disc
becomes drawn out into eight lappets, and the tentacles are then
thrown off. Each lappet contains one of the eight lobes which
have grown out from the ring-sinus; the lappet is forked at its distal
extremity, and in the re-entrant angle of each fork is the rudiment
of the sense-tentacle.

The next process which occurs is the separation of the " head " or
" crown " of the hydra-tuba from the stalk. This process is initiated

INVEBTEBEATA

CHAP.

by the appearance of a groove in the stalk ; it can take place, as
Friedemann shows, at different stages in the development, either
before or after the loss of the tentacles.

If food is scarce the crown separates as a free -swimming
organism termed an Ephyra, and the stalk slowly regenerates a
new crown ; but if food is abundant the process of the formation of a
new crown begins before the old crown has separated, and before it
is well under way a second groove appears below it, and a third
crown starts to develop; and by a repetition of the process the
Scyphistoina comes to look like a pile of plates, and is called a
Strobila. This process is known as strobilization, and in this way
one hydra-tuba can give rise to multitudes of Ephyrae (Figs. 52, 53).
The just liberated Ephyra is about an \ inch across the disc. The
wart-like sense-tentacles develop otoliths in their distal endodermal

cells, and this distal mass of
endoderm becomes separated
from the rest. The Ephyra
does not attain the characters
of the adult Aurelia until it
has grown to a size of at least

O

J inch in diameter. The
change in its shape, which
brings in the adult features,
consists in the slow growth of
adradial cushions, which are
situated between the bases of
the eight lobes of the Ephyra.

FIG. 51. — Two horizontal sections through the r,,, , • , ,, • ,1

upper part of a Hydra-tuba, about as old as These Cushions, by their growth,
that represented in Fig. 50, to show the gradually fill Up the deep re-

formation of the ostium connecting the entrant notches in the disc of

stomach pockets. (After Friedemanu.) , , ^ , , , •,

the Ephyra, and change its star-

vi /v j-i, J J

llke uutlme into the rounded
outline ot the adult Aurelia.
As each of these cushions grows, a new endodermal pouch grows
out from the ring-sinus and extends into it. At the same time
each endodermal pouch, which already occupies a lobe of the
Ephyra, becomes trilobed at its distal extremity. The median
branch of these three-pronged forks goes to the wart developed from
the base of the hydra-tuba tentacle once situated there. This wart
develops into the sense -tentacle of the Aurelia (Fig. 55). The two
lateral branches of the forks go into the two folds forming the forked
extremity of the Ephyra-lobe. These forks persist in the adult
as the curtains which eventually form a hood for the sense organ
of the adult. The oral cone becomes more and more prominent and
forms the maimbritim of the adult.

The genus Pelagia goes no farther than this stage. Each
adradial cushion develops a single long tentacle, and one only.
But in Aurelia, just as is the case with the Hydromedusan

A, above the level of the ostium. B, at the level of

the ostium; o*t, ostium.

IV

COELENTERATA

73

Podocorync (see p. 61), the eiuloderm of the radial ]x inches flattens
out so as to form plates which meet each other in the interspace
between two adjacent pouches, and thus form the so-called
cathammal plates, or, collectively, the endoderm lamella. In these
plates branches of the radial pouches hollow themselves out. Some
of these branches, at right angles to the pouches, form a circular
-canal just as happens in Podocoryne ; others form branches of the
per-radial and inter-radial pouches. The last i'< irmed adradial p< niches
do not branch. The numerous small tentacles which fringe the disc
of the adult, arise as sprouts from the circular canal (Fig. 56).

FIG. ~>'2. — Two stages in the strobilizatiou of the Scyphistoma of Ann-lin mii-itn.

(After Glaus.)

A, the appearance of the lirst transverse groove. B, tentacles lost, four transverse ,mo<>ves.
I, lobe of F.pliyra ; <>, oral cone ; /, taeniola ; ten. tentacle.

OTHER SCYPHOZOA

Hein (1903) has investigated the early development of another
genus Cotylorhiza. It agrees very closely with Aurelia, but the
original blastopore closes, and the mouth is formed later by the
reopening of this orifice. The temporary closure and subsequent
reopening of an orifice is to lie noted as a phenomenon of very
frequent occurrence in development; we interpret it as a sign
that the orifice in question is no longer continuously functional.

Pelagia is an instance of a form modified for oceanic life: it
develops a blastula like that of Aurelia, and a gastrula is formed by
iuvagination as in that animal; but the oiiginal blastoeoele persists
in the aboral end of the larva since the endodermic sac lemains

74

INVEKTEBKATA

CHAP.

relatively small. This

FIG. 53. — AstrobilizedScyphis-
tonia of Aurelia aurita.
(After Glaus.)

7, forked lappet of edge of disc
of Ephyra ; ten, tentacles of Hydra-
tuba degenerating ; Jen1, rudi-
mentary sense-tentacles of Ephyra.

again is a feature which we find in many
larvae which are adapted for continuous
free-swimming life. The larva never fixes
itself, and eventually the lobes of the Ephyra
grow out in a circle round the mouth.
The whole development is therefore modified
along quite similar lines to those exhibited
by the Geryonidae, the hydra-tuba being
modified into a floating larva, just as is the
hydroid stage of the Geryonidae.

When we review what we have learned
of the development of Scyphozoa, we are
struck at first by the great differences
between their life-histories and those of the
Hydrozoa. A deeper and closer analysis
tends, however, to diminish the supposed
differences very much. It has been shown
that many Hydroid colonies periodically
lose and regenerate the "polyps" (Allman,
1871-2), (i.e. the swollen distal ends or heads
of the hydroids which carry the tentacles
and genital organs), that during the winter
the polyps are often absent, and that these
are regenerated from the basal stumps in

FIG. 54. — An Ephyra larva of Aurelia aurita just after liberation from the strobilized

scyphistoma. (After Friedemami. )

ad, adradial lobe of ring-gut ; </./, gastral filament; int, inter-radial lobe of ring-sinus ; /, forked
lappet of edge of disc ; o.c, oral cone ; per, per-radial lobe of ring-sinus ; r, ring-sinus ; sg, sub-genital
pit ; toil, sense-tentacles.

IV

COELENTERATA

the summer. This is very much the same phenomenon as the
" strobilization " of the Soyphistoma, when the first " Ephyra-head "

is budded off.

ten

FK;. 55. — Longitudinal section through the sense organ of a young Ephyra.

mh-, calcareous concretions in the sense-tentacle ; 1, lobe of disc of Ephyra ; r.c, wall of radial canal ;

/<'//!, sense-tentacle.

Fin. 56'. — Three stages in the development of the Ephyra larva into the adult .1 urelia.

(After Claus.)

ad, adradial cushion; c.c, circular canal; g.f, gastral filament; I, lobe sheltering sens.' trutudi' ;
per, per-radial canal ; ten1, sense-tentacle. (The reference line without letter in I he' lirst li^uie points
to an inter-radial canal.)

Then in both groups the sexually mature person is typically a
person which breaks loose from the colony and develops a, swimming-
web. In Hydrozoa such a person breaks loose in such a, way as

76 INVEETEBEATA CHAP.

to leave practically no stump, but in Scyphozoa a stump is left
which can regenerate a new head. This is what the only differ-
ence, often much emphasized, between the formation of a medusa by
lateral budding and the formation of a medusa by transverse fission
consists in.

The fact that the sexual cells of Scyphozoa are discharged
inwards towards the stomach cavity, and not outwards as in
Hydrozoa, is a real difference. But it must he remembered that
it is confidently asserted that in many Hydrozoa with rudimentary
gonophores the sexual cells originate in the endoderm; and it may be
that they always have an ectodermal origin, but that in their first
stages they are indistinguishable from ectodermal interstitial cells.
Gastral filaments and septal muscles constitute, however, features
in which Scyphozoa n organization is higher than that of Hydrozoa.

III. ACTINOZOA

The great group of the Actinozoa, one of the four primary
groups of the Coelenterata, is distinguished from the Scyphozoa by
the replacement of the oral cone by an in turned, tube of ectoderm,
the stomodaeum.

The eggs of Actinozoa, like those of Scyphozoa, are developed in
the endoderm and dehisced into the coelenteron of the parent. In
most Zoantharia the embryos pass through the first stages of their
development within the body of the mother ; but in a few Zoantharia
and apparently in most Alcyonaria, the eggs are discharged through
the mouth of the parent into the sea and fertilized there. In this
case it is possible to obtain a great many specimens of the same age.
But when development takes place within the coelenteron of the
mother only a very few specimens of the earliest stages of development
will be found in any one individual parent, since these stages are
rapidly passed through. For this reason we select a Zoantharian
(Urticina crassicornis'), in which the eggs are discharged before
fertilization, as a type for special study in order to illustrate the
development of Actinozoa.

URTICINA CKASSICORN1S

Urticina crassicornis is a sea-anemone found on the British and
Norwegian coasts and its development has been worked out by
Appellof (1900). This observer kept the adults living in tanks in
the Bergen aquarium until they spawned ; he kept the eggs in
dishes of clean sea-water until the larvae hatched out, and these lie
was able to keep alive until they fixed themselves and metamor-
phosed into young sea-anemones. As preservative he used the
mixture of corrosive sublimate solution and acetic acid described
in Chapter II.

IV

COELENTERATA

77

The egg of Urticina when discharged is surrounded by a gelatinous
mass, through which presumably the fertilizing spermatozoon has to
penetrate. After fertilization this gelatinous mass hardens into a firm
capsule beset with spines, and within the shelter of this capsule the
early stages of development are passed through. The egg is composed
of a thin rind of relatively clear cytoplasm and an internal zone of
cytoplasm loaded with large spheres of yolk. The kernel of the egg
consists of a mass of material with sparse yolk spheres but with many
granules, which appears to be reserve food material not cytoplasm.

The egg is thus of the type called centrolecithal in Chapter I.,
and its segmentation is a matter of considerable interest. The zygotic
nucleus is- situated in tbe outer
clear layer of cytoplasm, and there
it undergoes its first division.
The daughter nuclei migrate into
the deeper layer of yolky cyto-
plasm and here undergo repeated
division until sixteen nuclei
have been formed, which are
distributed around the periphery
of the egg in the yolky layer.
Then and then only the cytoplasm
begins to be divided into blasto-
meres, of which consequently
sixteen are produced at once.
At first (Fig. 57) the blastomeres
are separated from one another
only at their outer ends, but
they soon become sharply de-
fined over their whole surfaces ;
nevertheless, even when so de-
fined, their inner ends are
embedded in the mass of reserve material which forms the innermost
core of the egg.

As segmentation proceeds a blastula is eventually formed, whose
wall consists of a single layer of small cells, but in whose cavity there
still remains the mass of " reserve -material " which formed the kernel
of the unsegmented egg (Fig. 58).

The blastula is at first ellipsoidal, but one pole becomes flattened
and in the centre of this pole an invagination takes place. The
manner in which this occurs is of great interest. The borders of the
patch which is to be invaginated bend in first, so that for a brief
period its central part projects like a knob. As the process of
invaginatiou proceeds the centre is also carried downwards nml
inwards, and thus a two -layered organism --i.e. a gastrula, is
produced. Occasionally the reserve material in the blastocoele persists
in considerable quantity ; it adheres to the centre of the area which
is normally invaginated and thus impedes the process of invagination.

;> ^>o£

crassicorms

FIG. 57. — An egg of

dividing into sixteen blastomeres. (After
AppelUif. )

lil, blast uim'ii's ; c, core of nutritive material in
the centre of the >"^ ; i.:, inner zone of yolky cyto-
plasm ; o.^, outer zone of clear cytoplasm.

78

INVERTEBEATA

CHAP.

This plug which normally persists for only a short time, persists in
this case much longer, and eventually the cells forming the borders
of the area of invagination are carried in past it, so that the
invaginated layer, or eudoderm, is represented by a solid plug of
material surrounded by a layer of cells. This plug is gradually

FIG. 58. — -Four stages in the development of the egg of Uftirina crassicornis as seen in
longitudinal sections. (After Appelldf.)

A, blastula. B, blastula preparing to undergo invagination. 0, invagination nearly complete,
gastrula stage. L), formation of stomo laeum lip, lilastopore ; c, remnants of the core of the egg ; end,
cndodiTin ; tin', area of invagination ; o, mouth ; stom, stomodaenm.

digested by the surrounding cells and thus the hollow gastrula stage
is reached.

The relation between the normal and abnormal methods of
reaching the two-layered stage in this species is the same as the
relation between the method of forming the planula larva in
Scyphozoa and that in Hydrozoa. We may regard them as two
varieties of gastrulation. The iuvaginated cells or endoderm,

IV

COELENTEKATA

form an inner sac which spreads till it completely displaces the food
material in the blastocoele, which is used up in nourishing the
growing cells. Both ectoderm and endoderm then co-operate in
producing a gelatinous secretion, the so-called jelly, mesogloea, or
supporting lamella. The cavity of the gastrula becomes the
coelenteron of the adult.

When the opening of the imagination has become narrowed so
as to form a slit-like blastopore, the ectoderm acquires cilia and the
embryo rotates within the egg-capsule, which shrinks and becomes
more transparent. A little later the embryo escapes from the capsule
altogether and swims about as a larva, but the swimming is not very
vigorous and the larvae do not rise far from the bottom.

-stem.

FIG. 59. — Two stages in the development of the larva of Urticina crassicornis.

(After Appelliif.)

A, free-swimming larva. B, stage just before fixation, ect, ectoderm ; end, endoderm ; m, mesenteries ;
p.o, post-oral region; o, mouth; stom, stomodaeum ; ten, tentacles.

The larvae are of ovoid shape with a broad aboral and a pointed
oral end. The aboral end is directed forwards in swimming, but the
reduced blastopore, which persists as the mouth, is not situated
actually at the oral end but a little to one side of it, so that there
is a small post-oral projection of the body. The ectodermal lips of
the blastopore grow inwards and form an inwardly-projecting tube
which is the stomodaeum (Fig. 58, D).

The mesenteries now make their appearance. The eight so-called
primary ones are formed about the same time. Each originates as a
fold of the eudoderm which projects inwards into the gastric cavity :
the cavity between the limbs of the fold being occupied by a layer of
supporting lamella secreted by the cells forming the fold. The
mesenteries correspond exactly to the taeniolae which occur in the
Hydra-tuba of the Scyphozoa, and which are irregularly developed
"even in the polyps of the Hydrozoa. The eight mesenteries are
arranged in four pairs, or, as it is usual to term them in this case,

80

INVERTEBRATA

CHAP.

stem

couples. Of these, one couple, which project into the post -oral
prominence of the larva, are known as the dorsal couple ; then follow
dorso-lateral, ventro-lateral and ventral couples. The ventro-
lateral couple develop more quickly than the others, they soon reach
the stomodaeal wall with which they fuse, and thus divide the gastric

cavity into a dorsal and a ventral
chamber. They also extend farther
towards the aboral pole of the
larva than the others, hut as
development proceeds all eight
fuse with the stomodaeum and
reach equally far towards the
aboral pole.

The chambers into which the
coeleuteron is divided by the
eight mesenteries are arranged as
follows. The dorsal chamber is
a median chamber at one end of
the long slit -like stomodaeum;
then follow a pair of dorso-lateral
chambers, then a pair of lateral
chambers, then a pair of ventro-
lateral chambers, and finally a
median ventral chamber, making
eight in all.

When the process of formation
of mesenteries is complete, per-
forations take place in the septa,
forming the so-called mesenterial
stomata, and thus the cavities
into which the coelenteron is
divided by the mesenteries are
placed in communication with
each other. In Urticina there are
two sets of these stomata, an inner
set near the stomodaeum and an
outer set near the outer body wall
of the larva. Both sets arise in
the same way ; the supporting
lamella becomes absorbed over a
limited area and the two layers
of cells which form the mesenterial

fold fuse with one another, and then in the centre of this area of fusion
absorption of the cytoplasm begins, and so a perforation is made
(Fig. 61). We may note that the taeniolae of the Hydra-tuba
larva become perforated in exactly the same way.

dl

FIG. 60. — Two transverse sections through
a larva of Urticina crassicornis to show
the formation of mesenteries. (After
Appellof. )

A, section through i>»st-oral region of larva.
B, section through middle of larva. <?.<-, dorsal
couplu of mesenteries ; </./, dorso-lateral mesen-
teries ; fil, mesenterial filament ; v.l, ventro-lateral
mesenteries; r, ventral mesenteries.

After

swimming

for about six weeks the larvae betnn to attach

themselves to the substratum by the aboral pole ; at first the attach-

IV

COELENTEEATA

81

stont

inent is only temporary, it is some considerable time afterwards that
a permanent attachment is effected and the pedal disc of the adult
formed. Before this occurs the rudiments of the first eight tentacles
make their appearance. Each arises as a simple outpouching of one
of the eight chambers into which the coelenteron is divided (Fig. 59, B),
and all appear to arise about the same time ; those belonging to the
dorsal and ventral chambers and to the lateral chambers are larger
than those belonging to the other four chambers.

The thickened edges of the mesenteries, where they end freely
in the coelenteron below the stomodaeum, are known as the
mesenterial filaments. In the adult Urticina each filament is
composed of a median strip of cells containing gland cells and
cnidoblasts, Hanked by two strips of cells carrying long cilia. The
inesenterial filaments appear on the ventro-lateral mesenteries long
before they appear on the others. They first appear in the neigh-
bourhood of the stomodaeum and grow downwards as simple streaks
of columnar epithelium ; then the central portion shows the
glandular modification of its cells, and much later the lateral portions
develop cilia. The other filaments make their appearance in the
same manner much later, when tentacles have already been developed.
According to Appellof, and
here he has the support of
other authors such as Gardiner
(1902), the filaments are com-
posed of ectoderm which has
grown down from the stomo-
daeum.

In Alcyonaria where, as in
the young Urticina, there are
eight mesenteries, two only
of these, the so-called dorsal
mesenteries, bear filaments
which carry cilia,— the other
filaments being purely gland-
ular in character whilst the
ciliated filaments are devoid of
gland cells. Following Wilson
(1883), who is the best
authority on Alcyonarian de-
velopment, the two dorsal fila- or supporting lamella; m.s, mesenterial stomata ; muse,
meiltS are USlially Said tO be Of muscular thickening on mesentery.

ectoderinal origin whilst the

others are stated to be endoderinal, but the evidence which he adduces

in favour of this view is, however, neither thorough nor convincing.

As the filaments are stated to close round the body of ingested
prey and to form a sort of temporary alimentary tube within the
coelenteron, and as their cells are stated to be the cells which secrete
the digestive ferment, one would at first -sight naturally expect them

G

muse

Fio. 61. — Transverse section through a, larva of
Urticina crassicornis in which the tentacles
have just been developed. (After Appdlnl'. )

Letters as in preceding figures. In a.MiUcm, j,

ov
VOL. I

82

INVERTEBBATA

CHAP.

stem

to be of endodermal origin. It is distinctly stated that in Alcyonaria
the two dorsal ciliated filaments do not take part in the process of
digestion, and if they are of ectodermal origin this is also what one would
expect. But if we accept Appellofs account of the development of
the filaments in Zoantharia, we must suppose that the ectoderm in
these animals has acquired digestive functions. Since in all groups
of the animal kingdom which have been carefully examined, the

distinction between pro-
tective ectoderm and
digestive endoderm is

O

the first physiological
differentiation to be
established, and the most
deeply rooted, one would
imagine it is unlikely
that Zoantharia should
in this respect form a
solitary exception.

But some observa-
tions by Miss Pratt on
the digestion of Alcyon-
aria (1905), appear to us
to place the whole matter
in a new light. She
finds that gland cells
similar to those found
in the six ventral diges-
tive filaments are found
also in the stomodaeum,
and that the tissues in
these filaments are so
similar to the stomodeal
tissue that she believes
that in Alcyonaria as in
Zoantharia all the fila-
ments originate from the
ectoderm. The effect of the digestive juice is not to dissolve the
bodies of the prey, but to break them up into granules, which are
then ingested whole by the endoderm cells covering the mesentery
beneath the filament. The cells forming the filament do not ingest
anything. It thus appears that this so-called ectodermal digestion
is merely a preparatory process similar to that exercised by salivary
glands in Mammalia, which, like the filaments, are of ectodermal
origin, and that in all cases the final digestion and the assimilation
are functions performed by the endoderm alone.

The muscular thickenings which run along the faces of the
mesenteries appear about the same time as the tentacles. The
supporting lamella becomes beset with branches on one side which

%••;-;

>r:>~-^e$^W>"-<\irWFW&
' 'i.-v.V' ••', '.ii^"^

FIG. 62. — Longitudinal section through the larva of
Ayaricia agar idles to show the ectodermal origin of
the mesenterial filament. (After Duerden.)

coe, coelenteron ; end, endoderm ; fil, mR^enterial filament ;
nerv, nervous tissue at the aboral end of larva ; nem, nernato-
cyst.

iv COELENTEKATA

are secreted by the overlying endoderm cells, these increase ill
number and develop basal longitudinal muscular tails. The muscles
h'rst appear on the venire-lateral mesenteries, and afterwards on the
others. Those on the ventral mesenteries are turned away from one
another, and those on all the other mesenteries are developed on that
side of each mesentery which faces towards the ventral mesentery of
its own side. It follows that the muscle thickenings on the dorsal
mesenteries are also turned away from one another.

The dorsal and ventral couples which are attached to the ends of
the stomodaeuni are known as directive mesenteries. In many
Actinozoa the ends of the stomodaeuni are developed into strongly
ciliated grooves — the so-called siphonoglyph.es or gonidial grooves.
In practically all, including all Alcyonaria, one end of the stomodaeuni
is thus modified ; this is called the ventral end, and to this end the
ventral directive mesenteries are attached.

The arrangement of muscle thickenings just described is the same
as that which persists for life in the family Edwardsiae, in which
family also, as in the young Urticina, there are only eight fully
formed mesenteries and eight tentacles. Urticina therefore passes
through an " Edwardsia " stage in development, and this has been
proved to be true of every Hexactiniau whose development has been
worked out.

In the very oldest specimens of Urticina which Appellof was
able to rear he found that extra mesenteries were being developed.
These extra mesenteries consist of two on each side, four in all, and
each of the new mesenteries was in such a position as to make a pair
with a ventro-lateral or lateral mesentery, and each bore a muscle
thickening facing the muscle of its fellow in the pair (see Fig. 67).
Such a pair, consisting of two mesenteries facing one another, is to be
carefully discriminated fiorn a couple, the two mesenteries forming
which are situated at symmetrical points on opposite sides of the
stomodaeuni.

Since the dorsal and the ventral couples of mesenteries may also
be regarded as forming two pairs, we reach in this way a total of six
pairs of principal mesenteries, and this is what is known as the
typical Hexactiniau arrangement, the most widely distributed
arrangement amongst Zoautharia. The powerful sphincter muscle
which in the adult closes the mouth was represented in the oldest of
the artificially-reared specimens merely by a thin sheet of circular fibres.

Appellof has also examined the development of a species of the
commonest genus of sea-anemones, Actinia. In this species, however
(Actinia equina), the earlier part of the development is passed through
in the coelenteron of the mother, and Appellof was unable to obtniu
a complete series of stages of this form ; however, one or two points of
interest were made out.

The endoderm originates by proliferation from the ectoderm cells ;
a proliferation probably confined to one pole. A hollow two-layered
planula larva is formed which is devoid of a mouth ; but a mouth is

84

INVEKTEBEATA

CHAP

formed later by the fusion of the two layers of the body wall at the
oral pole and their perforation at this point.

The larva possesses an anterior wisp of long cilia, the cells carry-
ing which are excessively attenuated and have all the appearance of
sense cells; and at their bases are a few rounded cells with tails,
obviously ganglion cells. In the larvae of Agaricia according to

•stem.

end

FIG. 63 — Stages iu the development of the larva of Actinia eqiiina. (After Appelliif. )

A, stage just before the formation of the mouth, the endoderm is already absorbed over the spot where
the mouth will be formed. B, stage when the mouth is formed. C, stage after formation of stomodaeum.
D, aboral pole of free-swimming larva much enlarged, ell, long aboral cilia ; n.f, nerve fibres. Other
letters as before.

Duerden (1902), although there is no bunch of long cilia at the aboral
pole, there is at this spot a comparatively thick layer of nerve fibres
(Fig 62).

In the species Actinia lermudensis, the development of which
has been worked out by Gary (1910), although the egg passes through
the earlier stages of development within the coelenteron of the
mother, yet the endoderm appears to be formed by in vagina tion

IV

COELENTERATA

85

just as in Urlicina crassicornis. On the other hand, in the species
Mctridium marginatum which has been examined by McMurrich
(1891), and Sagartia parasitica and Adamsia palliata, which have
been examined by Faurot (1903), although the eggs are expelled
from the mother previous to fertilization yet the endoderm appears
to be formed by proliferation from the outer cells of the embryo, that
is, from cells which become the ectoderm ; and in the two latter species
examined by Faurot this occurs at a very early period of development.
On the whole this method of forming the endoderm appears to be
much commoner than the method of invagination among Zoantharia,
and it is the only method recorded for Alcyonaria. In many cases
the endoderm cells are so swollen that, when the mesenteries appear,
the whole coelenteron is choked up by these cells and only slit-like
remnants of the cavity of the coelenteron remain.

The two families of Cereanthidae and Zoanthidae are formally
classed along with the Hexactiniae as Zoantharia, but they exhibit a
very different arrangement of mesenteries and in each case the egg
develops into a most character-
istic larva. A good summary of
what is known about the larvae
of both families is given by
Carlgren (1906).

The larva of the Cereanthidae
is termed Arachnactis, and it is
characterized by the excessive
prolongation of the free-
swimming stage. Two sets of
tentacles, an inner and an outer,
and numerous mesenteries are
developed whilst the larva still
continues to swim. Of these
mesenteries, there is a ventral
pair of " directives " attached to
one end of the stornodaeum, and
two "couples" attached to its
sides. The space which should be
occupied by the dorsal directives is
at first empty, but young mesen-
teries appear in it later, varying in
number with the age of the larva.
They are formed alternately to
the right and to the left of the
median line, and at first they are short, only later reaching the
stomodaeal wall.

The larva of the Zoanthidae appears under two varieties, in one of
which (Zoanthella) there is a transverse girdle of strong cilia, whilst
in the other (Zoanthina) there is a longitudinal band of cilia as
locomotor organ. It develops no tentacles until twelve mesenteries

FK;. 64. — The Arachnaetis larva of Cferamrf/iMS

membranaceus. (After Carlgven. )

86

INVERTEBEATA

CHAP.

have been formed, and then the twelve are developed in a single
cycle. The twelve mesenteries are arranged in six pairs which

correspond to the six pairs of Hexactiniae,
but the dorsal "directives" are short and
do not reach the stomodaeurn, and one
mesentery of each of the lateral and ventro-
lateral pairs remains short, whilst its fellow
is long and joins the stomodaeum. In the
space which intervenes between the ventral
"directives" and the ventro- lateral pair
on each side, there is a growing zone where
new pairs of mesenteries are added, one
fellow of each new pair being long and one
short.

It appears from this brief review that
the larvae of Cereanthidae, unlike the
Hexactiniae, do not pass through an " Edwardsia " stage in their
development, but that nevertheless they may be regarded as springing
from a stock, common to the Hexactiniae, Edwardsiae, and themselves,

FICJ. 65.— The Zoanthina larva
of a Zoanthid. (After
Carlgren.)

A

'cm

FIG. 66. — Transverse sections of Actinozoan larvae. (After van Benedi-n.)

A, section of Zoanthina larva. B, section of Arachnactis larva. <1, (in A) dorsal directive
mesenteries, (in B) iwlelinite number of mesenteries occupying the place of the dorsal directives ;
<i.Z, dorso-lateral mesenteries ; il.n, long dorso-lateral mesenteries ; il.l", short dorso-lateral mesenteries ;
v, ventral directive mesenteries ; v.l, ventro-lateral mesenteries ; r.n, long ventro-lateral mesenteries ;
v.l2, short ventro-lateral mesenteries ; .t-.r (in A) mark the places where additional pairs of mesenteries
are added.

in which only six mesenteries were developed. The Zoauthidae on
the contrary may almost be said to pass through a Hexactinian
stage in their development.

We have much less information on the development of Alcyonaria
than on that of Zoantharia. The best account is that of Wilson, to
which the more recent accounts by Koch of the development of
Gforgonia (1887), and by Hickson of the development of Alcyonium

IV

COELENTEKATA

(1901), have added nothing of any importance. Wilson worked on
the species Renilla reniformis and Leptogorgia virgulata (1883).
The eggs are expelled from the parent colonies and fertilized in the
sea. The endoderm appears to be formed by proliferation, and all
the eight mesenteries appear at once. The arrangement of the
muscular thickenings on these mesenteries differs only from that in
the Edwardsia stage of Hexactiniae, in the fact that the thickenings
of the ventral directives face each other instead of being turned away
from each other. Wilson's observations on the origin of the filaments
have already been dealt with.

The Alcyonaria differ less in this respect from the Edwardsiae
than these differ from the Cereanthidae, and the real ground of their
separation from the Zoantharia
lies in the method of forming
the skeleton, as will now be
made clear.

The popular name Sea-
Auemone is usually given to
those Zoautharia which do not
develop a calcareous skeleton,
whilst those which do form
skeletons are termed Coral -
forming Polyps — or briefly,
Corals. The development of
the skeleton in these was first
worked out by Lacaze-Duthiers

(1864), but the subject was FK;> 67.._Yoiing liying CaryophyWa cyathus

I

seen from above. The calcareous skeleton
shows through the transparent tissue. ( A fter
von Koch.)

Letters as in preceding figures. In addition, 8, one
of the primary septa ; tli, wall of theca.

again taken up and thoroughly
examined by von Koch (1897),
whose latest investigations
deal with the Mediterranean
species Gary opliy Ilia ci/atlius.

The first part of the skeleton to appear is the basal plate which
is secreted by the pedal disc of the polyp. This basal plate appears
as six separate areas of calcareous deposit, one area being situated
beneath the space intervening between each pair of mesenteries.
They eventually coalesce to form, first a six-rayed star and then a
circular disc. In the centre of each of the original areas the process
of secretion of calcareous matter continues more actively than else-
where, and the consequence of this is the formation of six radiating
septa of calcareous matter, each septum being covered by an inwardly
projecting fold of the pedal disc. The edge of the basal plate
becomes raised into a rim, owing to the upward extension ot the
skeleton-forming area on the side of the polyp, and in this way the
beginning is made of a theca or cup in which the polyp sits.

Both septa and thecal wall grow in height : soon a set of six
secondary septa alternating with the primary ones make their
appearance, whilst in the centre of the basal plate there appear two or

88

INVEETEBKATA

CHAP.

three small knobs which will later coalesce so as to form the columella.
The columella is the median pillar which projects upwards from the
base of the theca, indenting the base of the polyp. The primary septa
become extremely thick where they join the thecal wall. Still later,
cycles of tertiary septa make their appearance, and from the edges of
these structures isolated pillars become separated which form, the pali.
The skeleton of Zoantharian corals is therefore purely derived
from an external exudation, and in this respect it contrasts most
markedly with the skeleton of Alcyonaria. In his paper on Menilla
(1883), Wilson has described the origin of a typical Aloyonarian

FIG. 68.— Five stages in the development of tlie skeleton of Caryophyllia cyathus.

(After von Koch.)

A, the six primary areas of deposit coalescing to form a star-shaped figure. B, the thecal wall
just formed. C, the thecal wall thickened opposite the bases of the septa. D, the appearance of the
secondary septa and of the columella. E, tertiary septa formed, col, columella ; si, primary septum ;
s2, secondary septum ; s*, tertiary septum ; th, wall of theca.

skeleton. The lower cells of the ectoderm, corresponding roughly
in position to the interstitial cells of Hydra, acquire calcareous
concretions in their interior and migrate into the jelly. These
concretions form the characteristic Alcyonariau spicules. But in
llenilla, oval, wine-red, calcareous bodies are also formed in endodermal
cells, and both kinds of spicules are found in the adult. In their
characteristic skeleton therefore, as has already been said, lies the real
distinguishing mark of Alcyonaria.

IV. CTENOPHOKA

The fourth group of Goeleuterata differ profoundly from all the
rest, not only in their completely pelagic life, with no trace of a fixed

IV

COELENTEKATA 89

stage anywhere in their ontogeny, but also in the possession of a well-
developed nervous and sensory centre at the aboral pole, a part of the
body which in other free-swimming Coeleiiterata is the least sensitive
portion of the whole surface. The whole development is also of a
widely different type from that of other Coelenterata, so that at first
sight it is difficult to find any points of resemblance.

3 The most primitive type of Ctenophore known is that included in
the order Cydippidea. Unfortunately such forms cannot be regularly
obtained : occasionally they turn up in great swarms, and then for
years it will be difficult if not impossible to procure them. On the
other hand Bertie is a form which is abnormal in many respects, but
which can be obtained regularly in the Mediterranean, at least at one
season of the year, and it has been made the subject of much experi-
mental work. Two species of Bertie occur in the Mediterranean, JJ.
forskalii and B. ovata. The development of these two seems to be
'identical for all practical purposes and our illustrations will be
drawn from each.

BEROE

Beroe differs from primitive Ctenophora in possessing an
enormously expanded stomodaeum, recalling the cavity of the bell of
a medusa, and also in not having any vestige of tentacles.

We owe our first account of the development of Beroe to Chun
(1880), and his account has been supplemented by those of Driesch
(1895), Ziegler (1898), and Fischel (1897 and 1898), all of whom
approached the subject from the standpoint of Experimental
Embryology.

If Bertie be kept in an aquarium it will deposit its ripe eggs.
These are translucent spheres about 1 mm. in diameter, covered by a
tough membrane. They contain a large amount of food-yolk. The
nucleus is situated near one
pole (the upper), and at this
pole the most of the proto-
plasm of the egg is massed,
the rest of the egg consisting
of food-yolk.

Development goes on
within the membrane up to
the formation of a complete
larva, and owing to the

transparency of the eggS the FIG. 69.— Side view of the segmenting egg ..r .1
4- f 4-1 ^ ^^ Ctenophore (CaUianira bialata). (After

greater part of the develop- Metschnikoff.)

ment can be studied in the Qniy one Mf of ^ pgg jg ^ . ., js jn the 16.cell

living Object; but larvae stage, mm-, macromere; wtc, niicromeiv.

can be preserved in osmium

acid and embedded in celloidin and then examined by cutting
them into series of sections. The egg divides into two, and then
lour equal segments, by means of furrows which begin at the upper

90

INVEETEBEATA

CHAP.

pole and slowly make their way through the yolky portion of the
egg. The four segments then divide into eight, not as one finds in

B

mic

mic

ttltL

mic-

FIG. 70. — Two views of the developing egg of Bertie ovatn seen from above.

(After Ziegler.)

A, tint first-formed micromeres have just divided and a second micromere has burn lunlded off from
each macromere. B, the daughters of the tirst micromeres have divided again, win'1, daughters of
tirst-formed micromeres ; mic2, micromeres budded off subsequently.

other eggs by a circular furrow, but by oblique almost vertical furrows,

which separate off four inner larger cells from four outer smaller cells.

The eight cells are arranged in two linear rows of four each.

These rows stand opposite to one another and form an ellipse-like

A B

mac

Kii;. 71. — Oral and aboral views of the embryo of Bertie ovatn. in a later stage.

(After Ziegler. )

A, from aboral pule, li, from oral pole, mac, macromeres ; r, small ectoderm cells which later

will develop into the ribs of the adult.

figure, the long axis of which is at right angles to the stomach plane
of the adult, and is identical with the funnel plane of the adult
Ctenophore. These eight cells are termed the macromeres. Then each
niacromere, by unequal division, buds off a much smaller cell termed a
micromere at the upper pole, and thus a 1 6-cell stage is reached.
Now Ziegler (1898) has shown that the process of division of a

IV

COELENTERATA

91

r

•me.s

nies

blastomere takes nearly an hour to accomplish. During the process
of the division of the eight blasto-
meres into two tiers of cells, the
cytoplasm flows from the daughter
cell, which is originally the larger,
upwards into the smaller cell ; so,
by the time the division is accom-
plished the original proportions of
the two cells have become re versed, so
that what was originally macromere
is now micromere and vice versa.

At the next cleavage eight more
micromeres are budded off; this is
the division of the macromeres
of the 16-cell stage; and the first-
formed micromeres divide, and thus
the cleavage is complete, every cell
in the egg having divided, and a
total of thirty-two cells has been
reached. Each macromere with the
micromeres to which it gives rise,
may be termed an octant of the
egg. In Fig. 69 the egg of another
Ctenophore is shown in this stage
of development, seen from the Side.
All Ctenophora, the development
of which has been examined, seem
to agree in the way in which the
cleavage of the egg is carried out, and
this figure may therefore be taken as
representing what goes on in Beroe.

In the outer octants the division
of the first-formed micromeres is
unequal, the smaller daughter cell
being the smallest of all three
sets of micromeres, and the larger
daughter the largest of them ; the
new micromeres which have just
been budded from the macromeres
being intermediate in size. In the
middle octants the first -formed
micromeres divide equally.

In the next period of cleavage
the micromeres alone divide, the

stom

FKI. 72. — Illustrating the origin and fate
of the so-called mesoderm in a Cteno-
phore embryo (L'nllin nim bialata).
(After Metsehnikoff. )

A, view from oral pole at the time wh.-n the
" mesoderm " is being budded nil'. H. optical
longitudinal section of a slightly later stage.
showing rotation of the maerouieres and the
consequent invagination of the " mesodenn."
C, optical section of a still latiT stage, showing
accumulation of mesoderm at upper pole and
formation of stomodacum. I,e1ters as before.
mi'*, mnsoderm.

macromeres remaining quiescent.

The smallest micromere divides into two equal parts. Its sister cell
separates off towards the upper pole as a smallest tertiary micromere,
and, a^; all the daughters of the first-formed micromeres in the middle

92

INVERTEBEATA

CHAP.

octants likewise throw off a smallest micromere, there arises in this

way a crown of smallest
micromeres surrounding one
pole of the embryo.

At this stage the embryo
consists of fifty - six cells ;
eight niacromeres, and forty-
fight micromeres. The eight
macromeres now divide each
into two cells of equal size,
so as to form a circle of
sixteen large cells, and no
further divisions take place
in them until the micromeres

stem

have completed their
multiplication.

In subsequent divisions
in the

FIG. 73. — Optical section of embryo of Bertie
forskalii, showing the beginning of the endo-
dermal cavities. (After Chun.)

end, parenchyma-like endoderm ; r, rib; stom, stomo-

daeum which forms the so-called "stomach." Cells divide first and then

the larger micromeres divide.

In the middle octants also the four smallest micromeres divide first,
whilst the eight larger micromeres flatten out and commence to spread
over the macromeres, after which they also divide. From this time
on, division of the micromeres
occurs rapidly, and the sheet of
cells to which they give rise
spreads more and more over
the surface of the macromeres.
The macromeres are originally
exposed both above and below
but the upper opening is nar-
rowed as the edge of the ring
of smallest micromeres extends
inwards, whilst the larger
micromeres rapidly extend
downwards over the surface of
the macromeres. This over-

stom

spreading of the macromeres by Fla. 74,-Opticai section of embryo of

forskalii in a later stage of development,
with a hollow endodermal sac. (After Chun. )

Letters as before. In addition, ap, apical nervous
plate ; ot, otolithic concretions.

smaller cells is termed epibole.
It is a process often met with
in the development of animals
and is to lie regarded as a variety
of gastrulation.

There can now be seen, radiating from the upper pole,
four streaks of specially small and rapidly dividing cells; these
are the forerunners of the "ribs "of the adult which carry the
comb-like plates of cilia. Each streak corresponds to a pair of ribs.

IV

COELENTERATA

93

Just before the lower pole of the macromeres is completely covered
by the advancing ectoderm, each macromere bud* off downwards,
a small cell. We thus get a circle of sixteen small cells at the

A

-S.fen

FIG. 75. — Two optical sections through the embryo of BeriJe forskalii. (After Chun.)

A, through the stomodaeum. B, above the stomodaeum near the aboral pole. •
end, cavity of the gastric sac. t, taeniola.

vegetative pole ; these are the rudiment of the so-called mesoderm.
The macromeres now rotate in such a way that the " mesodermal "
cells are rotated upwards
and inwards, and eventu-
ally come to lie at the
upper pole of the macro-
meres. Here they undergo
rapid division and form a
cross, the two longer arms
of which extend in the
direction of the long axis
of the embryo, while the
two shorter ones are trans-
verse to that axis (Fig. 72).
The ectodermal skin
is now completed, and the
macromeres now undergo
rapid division, forming a
parenchyma - like tissu e.
Between ectoderm and
endoderm jelly appears
as a secretion; and into
this jelly wandering cells

are budded from the CrOSS The paragastric canals have forked and united at x with

of "mesoderm" Cells. the sub-ventral or sub-" stomachic" canals. The sub-tentac-

These cells become con- ular ca"a!s are f11 short Lfters as,befof -forks°f

paragastric canal; p.g, paragastric canal; s.st, sub-stomachic
nected With One another, canal ; g.«ew, sub-tentacular canal.

with the ectoderm and

with the endoderm by their processes, so as to produce a cell-network

which simulates connective tissue ; it is, however, certain that many,

FIG. 76. — Larvu of BeroeJ'vfxki'Hi four days old, viewed
from "stomach-plane." (After Chun.)

94 INVEKTEBRATA CHAP.

if not most, of the cell -processes are contractile, and therefore these
wandering cells are to be regarded as muscular.

In the eiidoderm there appear slit-like spaces between the cells
here and there, and these now coalesce so as to form a single roomy,
gastric cavity. At the lower pole the stomodaeum now makes its
appearance as an invagination of the ectoderm. This, as it grows
upwards, indents the endodermic sac and constricts it into right and
left halves. An indentation occurs in this sac at each side of a line
which is at right angles to the plane of the stoniodaeum, and in this
way a four-lobed sac is formed. We might with perfect justice
describe the process as a formation of four ridges or taeniolae, which
grow into and indent the cavity of the endoderm sac.

Meanwhile, the " combs " of cilia have appeared in the regions,
where, at an earlier stage, the streaks of rapidly-dividing ectoderm

C3C

esc:
s.st

FIG. 77. — Part of apical region of larva of Be roe forskalii, viewed from stomacli-plaue.

(After Chun.')

Letters as before. e.c, excretory vessel rising from the funnel.

cells were noticeable. Thus the ribs of the adult are established. At
the upper pole, groups of stiff cilia supporting otolithic masses are
formed, and in this way the apical sense-organ is completed.

We have now an oval embryo containing a four-lobed gastric sac,
whose walls are formed of vacuolated cells with stiff membranes, and
having on one side a mouth leading into a flattened stoniodaeum
which projects inwards into its interior. Eunning like the meridians
on a globe are eight ribs of thickened ectoderm, each bearing a series
of combs of cilia, and converging to a polar plate at the pole opposite
the mouth : this plate carries groups of stiff converging cilia which
support an otolith where they meet.

At this stage the embryo escapes from the egg-membrane and
begins life as a free-swimming larva. The later history has been
followed only by Chun and has been deduced from the examination of
specimens caught by the Plankton net. From these he concludes
that the meridional canals appear on the periphery of the endodermic
pouches as everted grooves. First the sub-tentacular and then the
sub-stomachic canals appear, then the two paragastric canals arise as

IV

COELENTEKATA

95

independent evaginations. All grow down towards the edge of the
mouth and here each one forks, and adjacent forks unite with one
another, and so a circular canal is formed. This is a peculiarity
of Berue as opposed to other Ctenophora. From the gastric sac
two canals extend upwards towards the aboral pole of the larva and
fuse with the ectoderm at the sides of the apical plate. Here open-
ings are made to the exterior. These canals are called excretory
canals, and out of them a current of water flows (Fig. 77). It is
probable that this current forms the exhalent portion of°a respiratory
current, and that water enters
by the mouth to replace it.
Finally, the meridional canals
give off short outgrowths
which, in one species, anasto-
mose with one another so as
to form a network.

CALLIAN1KA

The main difference
between the development of
Beroe and that of other Cteno-
phora lies in the presence of
tentacles more or less modified
in the other groups.

The best account of the
development is that given by
Metschnikoff of Callianira
(1885). From this account
we learn that the two main
arms of the " mesodermal
cross," after having given off
a certain number of wander-
ing cells, give rise to the tissue
which forms the axis of the
tentacles. The tentacles themselves appear as invaginations — the
tentacle pockets — from the base of which the real tentacle sprouts.
These tentacle pockets indent the endodermic sac in a plane at right
angles to that in which it is indented by the stomodaeum.

m

FIG. 78. — The free-swimming larva of (J«llitniii-n
liinlata viewed from the stomach-plane. (After
Metschnikoff. )

tun, freely projecting tentacle ; //«/, wandering cells
with contractile processes.

AFFINITIES OF CTENOPHORA WITH OTHER COELENTEliATA

Now, when we review the account which has just been given of
the development of Beroe, there is really only one point where any
marked similarity with the developmental stages of other Coelenterata
shows itself, and this is when the ectoderm has completely invested
the macromeres, and these latter have broken up into a mass of cells
like plant " parenchyma," with only slits between them. This staye

96 INVEETEBRATA CHAP.

recalls the solid planula stage of other Coelenterates, the slit-like
spaces being comparable to the incipient absorption spaces which
are the first stage in the formation of the gastric cavity in other
Coelenterates.

Perhaps we might go farther and find in the stage which succeeds
to this a similarity to Actinozoon development. In the development
of Actinozoa an ectodermal stomodaeuni is also formed, and the
primary lobing of the enterocoelic sac by four folds in Bertie might
be compared to the outgrowth of taeniolae or septa in Actinozoa.
There would, however, remain an irreconcilable difference, viz., that
the first tentacles in Actinozoa sprout from the pouches, whereas
in Ctenophora they occur between them — for in Ctenophora, as we
have seen, the tentacle pockets cause the formation of taeniolae and
therefore alternate with the pockets of the gut.

Reverting, however, to the planula stage common to all Coelen-
terates, a comparison of the later history of this stage in the various
groups reveals the real relationship of the Ctenophora to the rest.
In Hydrozoa, Scyphozoa, and Actinozoa, the planula, after a brief
period of swimming, fixes itself by its aboral pole, which becomes
the root of the future colony ; but in Ctenophora the planula never
fixes itself but remains free-swimming and develops a complicated
sense-organ at the aboral pole.

Hence, if all Coelenterata have sprung from a planula-like
ancestor, the Ctenophora must represent a branch which never deserted
the free-swimming life, and which in consequence must represent the
main stem of Coelenterates, while the other groups, though far more
abundant at the present day, must represent degenerate offshoots
of this stock. Of these we may suppose that the Actinozoa represent
a group which assumed a bottom life later than the rest, and in which,
consequently, evolution had gone farther, and a stomodaeuui had
been formed. In accordance with this conclusion we find that
Ctenophora present resemblances to the larvae of the higher forms
in far greater degree than do other Coelenterata, for it is to be
expected that higher forms would arise from a dominant free-
swimming group rather than from a degenerate sessile one.

EXPERIMENTAL EMBRYOLOGY OF COELENTERATA

But though in their later larval life the Ctenophora retain many
primitive features, in their earlier embryonic life they have undergone
great specialization. This will be made clear by contrasting the
results obtained by Zoja (1895-1896), who experimented with the
eggs of Hydromedusae, and those obtained by Driesch (1895) and
Fischel (1897-1898), who experimented with the eggs of JBeroe.

Zoja, worked with the genera Liriope, Geryonia, Mitrocoma, Clytia,
and Laodice, and he separated the first blastomeres of the segmenting
egg with a needle. In the case of Clytia and Laodice he found that
a single blastomere of the 16 -cell stage was capable of developing

IV

COELENTEBATA

end

into a normal planula, and that in all cases one of the first four
blastomeres could do so. From such a blastomere in Clytia a hydroid
was reared, and in Liriope a fully - developed medusa with four
tentacles was reared.

Now Driesch and Morgan (1895) made a number of experiments
on the eggs of Beroe of which the most interesting are these. By
means of a fine scalpel they cut pieces from the unsegmented egg. Such
mutilated eggs mostly died, but about sixteen out of five hundred
survived, and eight of these developed into larvae with a diminished
number both of ribs and endodermal pouches.

From this experiment Driesch and Morgan draw the conclusion
that the material required to
form definite regions of the
embryo is localized in definite
parts of the egg. This con-
clusion is amply confirmed by
the result attained from separa-
tion of the first blastorneres of
the egg by means of a scalpel.
Each of the first two blastomeres
produces an embryo with four
ribs. Each one of the first four
blastomeres forms a larva with
two ribs only; and further, when
one blastomere is separated
from the first four the remain-
ing three blastomeres form an

pinlivvn with <siv riV>Q FlG- 79.— An embryo of BerHc mala with four

ti 1 1 I I.'J. y \J V\ J. u Al oJ. jV J. J. L^o« -i i. ii -t i j

J. nr\H -i nnr>\ • '' a *wo en('ot'erinal pouches, and a

V ISChel (1897-1898) im- small extra third pouch ; obtained by isolat-

pl'OVed On Driesch and Morgan's ing one of the first two blastomeres of

methods: he separated the
blastomeres from one another
by subjecting the egg to pres-
sure, and by pinching the egg-
membrane with forceps. By this means he found he could make one
embryo produce three smaller embryos with a lessened number of
ribs, and he found that the united number of their ribs amounted
to the total of a normal embryo. By pressure he also separated
the smallest rnicromeres, i.e. those which give rise to the apical
plate, into two portions, and from these resulted an embryo with
two apical plates. When pressure was applied in later stages the
result was, not to produce several larvae with a lessened number of
ribs, but to break up the ribs already formed into several pieces.
In larvae with four ribs, produced from one of the first two blastomeres,
three endodermal pouches are formed, not two as one would expect
(Fig. 79). But Fischel points out that whereas the first two are
produced by the ingrowth of taeniolae in the tentacle plane, the
small third one owes its origin to the fact that the stomodaeum
VOL. i H

end, one of the two normal endodermic pouches ;
emi', the small extra endodermic pouch ; r, the four
ribs. The other letters as before .

98 INVERTEBRATA CHAP.

originates close to one side of the larva, not at the absolute edge as it
should do were the embryo a perfect half; in consequence of this
fact the growing stomodaeum indents the endodermic sac unevenly,
cutting off a little third pouch.

From the fact also that in this half larva, on the side next where
the missing half should be, the endoderm is not naked but covered
with ectoderm ; and from the fact that by separating the lower
ends of the macromeres he succeeded in producing a form with two
stomodaea, Fischel concludes that although the material destined to
form the specialized ribs and the apical plate is originally rigidly
localized in the germ, this is not the case with the rest of the ectoderm.
This unspecialized ectoderm spreads till it covers all the exposed
macromeres, whilst the stomodaeum is formed owing to the action
on this general ectoderm of a stimulus proceeding from the lower
ends of the macromeres.

From a review of the work of all these experimenters we draw
• the conclusion that in the eggs of Hydro medusae, up to the 16-
cell stage, the part resembles the whole in its constitution ; and the
question whether one portion shall form only part of an embryo or
whether it shall form a whole embryo, depends on whether or not it
remains in connection with its fellows. In Ctenophora, however, we
must conclude that the part is quite different from the whole, and
that the parts destined to form the ribs and apical plate are mapped
out even in the uiisegmented germ ; these parts must, therefore,
be represented by portions of the cytoplasm of the egg, not by nuclei.

The egg is incapable of regenerating a lost part, but in this
respect a remarkable observation of Chun's (1880) must be borne in
mind. He experimented with the eggs of Bolina and obtained half
larvae just as did Driesch and Fischel with Beroe. But Chun kept
his half larvae living for weeks, till they developed generative organs
on their meridional canals, and he states that the missing half was post-
generated. This observation has been recently confirmed by Mortensen.

That an animal in its young stages should possess no powers of
regeneration, but should acquire them when it is older, is a curious
fact but not unprecedented, for the same thing occurs in Ascidians.
We have seen that the specialization of the egg for the formation of
organs is a specialization of plasma, but it will be shown later in this
volume that this specialization must lie regarded as due to an
influence emanating from the nucleus of the ovum during the period
of its growth and ripening. We must, I think, attribute the
secondarily acquired power of regeneration to a reorganization of the
cytoplasm, due to renewed influences emanating from the nucleus.

ANCESTRAL MEANING OF THE PLANULA

We have now to consider the meaning of the development of
the planula. We have already put forward the hypothesis that
the planula represents a free-swimming ancestor common to all

iv COELENTEEATA 99

Coelenterata. Now the planula appears under two forms : in
Scyphozoa and in some Actinozoa as a hollow two-layered vesicle
with a terminal opening, and in Hydrozoa and many Actinozoa
as a solid mass of endoderm surrounded by a skin of ectoderm.

Which of these two is the more primitive and which the derived
form ? In answer to this question we say at once, the first of these is
the more primitive, because it alone exhibits a structure which is
a physiological possibility for a self-supporting animal. A solid
internal mass of cells would be quite functionless in an animal that
had to get its own living.

The stage of the planula in development is preceded by the stage
of the hollow blastula, in all cases which have been thoroughly ex-
amined. The hollow blastula is changed into the planula either («)
by intucking or invagination of one end, (&) by active proliferation of
cells proceeding from one end and filling up the interior, or (c) by
proliferation of cells from the whole internal surface. We have
already pointed out that, whereas (c) is described only in cases of
eggs developing rapidly inside the bell of a vestigial medusa, or
with a shortened development in which the hydroid stage is almost
eliminated and the egg develops directly into a medusa, and that
the assertion of its occurrence even in these cases may be based on
a mistake in the observations ; on the other hand (a) and (&) occur
in eggs with a long larval development.

We may take it therefore that these latter methods of eudoderm
formation represent the least modified form of development, and that
the ancestral blastula was developed into the ancestral planula by a
proliferation of cells at one pole only, or by an invagination of the
cells forming the wall of the blastula at this pole.

If this be admitted, however, we have no difficulty in deciding
that invagination must be more primitive than polar proliferation.
Our reason for that decision is that polar proliferation would be
meaningless in an adult animal, whereas invagination means, primarily
an increase in surface area of a portion of the animal, and secondarily
an inbeiiding and the consequent continuous preservation of a
cavity between the invaginated cells, which cavity is destined to
contain food.

In fact, as Korschelt and Heider point out, .a ciliated animal,
progressing forward in one direction, tends to create suction behind
it, so that particles struck backwards by the cilia tend to accumulate
there ; just as may be observed at the tail of an express train as it
dashes past a station. Here then would be sufficient inducement
for the tendency to increase and exaggerate the function of ingestion
—a function which all the cells of the planula originally must have
possessed, — and so we may suppose that an endoderm and an ectoderm
would become specialized from an indifferent layer of cells.

As the endoderm cells increased in number it became necessary
that they should find room, and this they did by bending inwards,
and so the planular stage is reached. When this stage is repeated

100 INVEETEBEATA CHAP.

in ontogeny, and when the food necessary for the embryo is stored
up within its cells in the form of yolk-grains, and has not to be
sought for outside, then the inbending can be replaced by solid pro-
liferation because the larval gut is no longer a functional organ.

We are thus led to form the following conception of the past history
of the lower Metazoa. A widespread and dominant race of blastula-
like animals once swarmed in the primeval seas. Some of these
took a creeping life and eventually gave rise to the group of sponges ;
others kept to the free-swimming life and developed into planulae,
and so gave rise to the Coelenterata. Some of these planulae, by the
specialization of the cilia into comb-like locomotor organs, became
Ctenophora ; whilst the remainder adopted a fixed life and attached
themselves by their aboral poles. This change occurred in different
divisions of the stock at different stages of the evolution of the
internal organs of the planula ancestor, and in this way the groups
of Hydrozoa, Scyphozoa, and Actinozoa arose.

LITERATURE REFERRED TO

Allman. A Monograph of the Gyrunoblastic or Tubularian Hydroids. Ray Society,
1871 and 1872.

Appellbf. Studien iiber Actinieii-Entwickhmg. Bergens Museums Aarbog, 1900.

Brauer. Uber die Entstehung der Geschlechtsprodukte mid die Entwicklung von
Tubular la mescmbryanthemum. Zeit. fiir wiss. ZooL, 1891.

Carlgren. Actinien-Larven. Nordisches Plankton, 5te Lieferung, 1906.

Gary. The Formation of the Germ-layers in Actinia bermudensis. Biol. Bull.
(Wood's Hole), vol. 19, 1910.

Chun. Fauna und Flora des Golfes von Neapel. Ctenophora, 1880.

Chun. Zur Morphologic der Siphonophoren. Zool. Anz., vol. 10, 1887.

Dalyell. Rare and Remarkable Animals of Scotland. London, 1847.

Driesch and Morgan. Zur Analyse der ersten Entwicklungsstadien des Cteno
phoreneies. Arch. Eut. Mech., vol. 2, 1895.

Duerden. West Indian Madreporarian polyps. Mem. Ac. Washington, vol. 8, 1902.

Faurot. Developpement clu pharynx, des couples et des paires de cloisons die/ les
Hexactiniidae. Arch. Zool. Exp. (4me serie), vol. 1, 1903.

Fischel. Experiraeutelle Untersuchungen am Ctenophorenei, I. Arch. Ent.
Mech., vol. 6, 1897. Do. II. Arch. Ent. Mech., vol. 7, 1898.

Friedemann. Untersuchungen iiber die postembryonale Entwicklung von Aurelia
aurita. Zeit. fiir wiss. Zool., vol. 71, 1902.

Gardiner. Flabcllum, Anatomy and Development. Marine Invest. S. Africa. Cape
Town. 1902.

Gotte. Vergleichende Entwicklungsgeschichte der Geschlechtsindividuen der
Hydropolypen. Zeit. fiir wiss. Zool., vol. 87, 1907.

Haeckel. System der Siphonophoren auf phylogenetischer Grundlage. Jen. Zeit.
Nat., vol. 22, 1888.

Harm. Die Entwicklungsgeschichte von Clara squamata. Zeit. fiir wiss. Zool.,
vol. 73, 1903.

Hein. Untersuchungen iiber die Entwicklung von Aurelia aurita. Zeit. liir wiss.
Zool., vol. 67, 1900.

Hein. Untersuchungen iiber die Entwicklung von C'o/i/JnrJ/t'-a tubcrculata. Zeit.
fiir wiss. Zool., vol. 73, 1903.

Hickson. Alciioninm, Liverpool Mar. Biol. Com. Memoirs. No. 5, 1901.

Huxley. Oceanic Hydrozoa. Publications of Ray Society, 1859.

von Koch. Die Gorgoniden. Fauna und Flora des Golfes von Neapel, etc. No. 15.
1887.

von Koch. Entwicklung von Caryqphyllia cyathits. Mitt. Zool. St. zu Neapel,
vol. 12, 1897.

iv COELENTERATA 101

Korschelt and Heider. Lehrbuch der vergleichenden Entwicklungsgeschichte der
wirbellosen Tiere. Vol. I. Jena, 1890.

Lacaze-Duthiers. Histoire iiaturelle du corail. Paris, 1864.

McMurrich. On the Development of Hexactiniac. Joiirn. Morpli., vol. 4, 1891.

Metschnikoff. Vergleinhende embryologische Stndien, II. Zeit. fur \viss. /mil.,
vol. 36, 1882. Do. IV. Zeit. f'iir wiss. Zool., vol. 42, 1885.

Metschnikoff. Embryologische Studien an Medusen. Ein Beitrag zur Genealogie
der Primitivorgane. Wien, 1886.

Pratt, E. M. The Digestive Organs of the Alcyonaria and their Relation to the
Mesogloeal Cell-])lexus. Quart. Journ. Mic. Sci. , vol. 4, 1905.

Rittenhouse. The Embryology of Stomotoca apicata. Journ. Exp. Zool., vol. 0,
1910.

Wilson, E. B. The Development of Renilla Phil. Trans. Roy. Soc. (Lend.),
vol. 174, 1883.

Ziegler. Experimentelle Studien iiber Zellteilnng, II. Arch. Ent. Mech., vol. 7,
1898.

Zoja. Sullo sviluppo dei blastomeri isolati delle nova di alcune meduse. Arch.
Ent. Mech., vol. 1, 1895 ; vol. 2, 1896.

CHAPTER V

PLATYHELMINTHES

Classification adopted —

Platyhelminthes

Turbellaria

Trematoda

. Cestoda

_. , . f Polyclada
f Dendrocoela { Triclada

| I Acoelida

Ehabdocoela -j Rhabdocoelida
[ Alloiocoelida

THE phylum of Platyhelminthes or Flat -worms agrees in one
point of structure of great importance with the Coelenterata. The
alimentary canal may, it is true, entirely disappear in some members
of the phylum which are internal parasites and which live Ly the
absorption of fluids through the skin, but when it is present it has
only a single opening, the mouth, which serves both for ingestion
and egestion. Further, between alimentary canal and skin there is
no real body-cavity, the space being occupied by a ground substance
comparable to the jelly of a Coelenterata. This ground substance is
invaded by numerous stellate cells connected together by their pro-
cesses, some of which become muscular and contractile ; in these
two respects this tissue resembles especially the jelly of a Ctenophore.

When we survey the development of the eggs of this group, we
find a feature common to a large number which entails modifications
of the early life -history of a far-reaching character, and renders
observation correspondingly difficult. This peculiarity is that the
eggs are enclosed in large numbers in a common capsule, and that of
this number only one is destined to develop into an embryo, whereas
the rest, termed " vitelligenous," i.e. yolk-bearing cells, are destined
to become its food.

Now, as a result of this arrangement, the earlier stages of
development are modified out of all recognition. The first -formed
blastomeres are stated to separate from each other completely, then
to wander to the periphery of the vitelligenous cells, which they
surround, and then to join together to form an embryo. In fact

102

CHAP, v PLATYHELMINTHES 103

one could not have a better example of the disturbing influence of a
superabundance of food, which we have already seen reason to
believe is one main cause of variation.

Now it is obvious that these peculiarities are secondarily
derived, that they are not primary characteristics ; yet they range
throughout the entire groups of the Trematoda and Cestoda, and in
the group of the Turbellaria they are found in Triclada amongst
Dendrocoela, and in Ehabdocoelida and Alloiocoelida amongst
Khabdocoela. In the curiously modified Acoelida, where the gut
has no lumen and its cells are indistinguishable from those of the
parenchyma, this peculiarity does not occur, nor does it occur in the
group Polyclada of the Dendrocoela.

Now the Acoelida support life, as Keeble (1907) has shown, by
means of their association with a plant ; this accounts for the
absence of a hollow alimentary canal, and it cannot therefore be
regarded as a primitive feature. The Polyclada, on the other hand,
retain the power of swimming by cilia, and they exhibit other
features of a very primitive character ; it is to their ontogeny, there-
fore, that we naturally turn for light on the origin of the group.

The pioneer in this work has been Lang (1889), who has worked at
the development of several European genera. We nevertheless take for
type the American form Planocera, which has been worked out with
great care by Surface (1907), because it is the most recent work and
the most modern methods have been employed for it, whereas Lang's
work dates back twenty to thirty years. Nevertheless the outcome of
Surface's work is to support Lang's main conclusions, and to suggest
strongly that the eggs of all the genera of Polyclada segment very
much in the same way, so that what is here recorded of Planocera
will be found to be nearly correct for the European species also.

PLANOCERA

Planocera lives in the mantle-cavity of the Gastropod Sycotypus.
It does not feed — so far as is known — on the tissues of its host, but
uses its host's mantle-cavitv as a convenient retreat. It is therefore

<j

a commensal, not a parasite. The adults were obtained by opening
the branchial cavities of specimens of the Gastropod. They were
kept in vessels containing clean sea-water through which a current of
air was allowed to bubble. They laid their eggs in these vessels, and
the eggs lived till the free-swimming larva escaped.

The eggs of Planocera are minute, being only '1 mm. in diameter,
and they are laid in capsules, usually only one in each capsule, and
the capsules are embedded in a gelatinous slime. Occasionally two
eggs are laid in a capsule, and then both become normal embryos. No
attempt was made by Surface to extract the eggs from the capsules,
but they were examined living and were then preserved in fluids of
penetrating power which reached and preserved them whilst still in
the capsules.

104 INVERTEBRATA CHAP.

The preserving fluids employed with most success were a mixture
of 3 parts corrosive sublimate and 1 part acetic acid dissolved in 95 per
cent alcohol ; and Gilson's fluid — a mixture of corrosive sublimate and
nitric acid. Other fluids were tried but did not give good results.
The preserved eggs were stained in Grenadier's haematoxylin, and
cleared in xylol and mounted in Canada balsam. The operation of the
clearing agent was facilitated by piercing the capsule with needles.

The embryo develops within the capsule until the sixth day,
when it escapes as a free-swimming larva of a peculiar type known
as Mliller's larva. This larva swims about at the surface for some
time, but eventually sinks to the bottom and then takes on the form
and habits of a Polyclade.

In the development of Planocera we meet for the first time with
what is termed " spiral cleavage " of the egg. This type of segmen-
tation of the egg into blastomeres is very widely distributed. It is
found in all Polyclada which have been studied, it is universal
amongst Annelida, and it is found in all Mollusca except Cephalo-
poda. In the Neuiertine worms it also appears, though in a very
primitive form. Developments of this type have been studied in
great detail by zoologists of the American school, and they have
invented a nomenclature which is applicable to all such develop-
ments ; we shall endeavour to make this clear, and shall adopt it in
the description which we give. The object aimed at in these studies
is to trace back definite organs of the embryo or larva to individual
blastorneres of the egg in its early stages of cleavage. This is termed
tracing the Cell-lineage of the organs.

The general features of "spiral cleavage" are these. The egg
divides as usual into two and then into four cells, by two cleavage
planes at right angles to one another. These four cells then divide
into eight, which lie in two tiers of four, one above the other. So
far there is nothing peculiar about the type. But the four cells nearest
the animal pole of the egg are usually much smaller than the
others, and are termed micromeres, whilst their larger sisters are
termed macromeres. Further, the spindles by which the nuclei of
the micromeres are separated from those of the macromeres are not
vertical but oblique, with the result that the micromeres are situated
opposite the furrows between the macromeres, and, so to speak,
alternate with them.

In Planocera, and in the great majority of cases of spiral cleavage, in
the transition from the 4- to the 8 -cell stage, each spindle is so
inclined that the micrornere lies at the upper right-hand corner of the
macromere from which it has separated (compare 1A and la in Fig.
80) ; that is, the upper right-hand corner when viewing the egg from
above the animal pole. Such a direction of cleavage is termed
dexiotropic. In only a few cases, in which reversed cleavage, as it
is called, occurs, the spindles preparatory to the formation of the
8-cell stage are so directed that the micromere lies at the left-hand
upper corner of the macromere. Such cleavages are termed laeotropic.

V

PLATYHELMINTHES

105

la

\b

1A-

Ic

Id

The 8-cell stage is succeeded by a IG-cell stage. The micro-
meres divide into upper and lower cells by laeotropic spindles,
and by four laeotropic spindles
four new micromeres are budded
off which alternate with the lower
daughter cells of the first micro-
meres. (Fig. 81.)

The IG-cell stage is succeeded
by a 32 -cell stage. By dexio-
tropic spindles the macromeres
bud off a third set of micromeres.
The second micromeres divide
into upper and lower cells, whilst
each daughter of the first set of
micromeres divides into an upper
and lower cell.

The Subsequent history of the FlG> 80.— Developing egg of Planocera
i ,-, • 7-,j inqwiMna. Eight - cell stage viewed

embryo proves that 111 Planocera, from animal pole. (After Surface.)

as in every Annelid and Mollusc

that has been examined, the three groups of micromeres and their
daughters constitute the entire ectoderm, whilst what is left of the

macromeres, after the separa-
tion of these micromeres,
gives rise to the endoderm
and mesoderni.

Now if the four macro-
meres were precisely equal in
size it would be of course im-
possible to distinguish them
from one another, but in
Planocera, as in the vast
majority of cases, one is
slightly larger than the rest
and distinguishes itself by
peculiarities in its develop-
ment after the micromeres
have been given off; this

macromere is denominated D.

FIG. 81.— Developing egg of Planocera inquilina. T 11 where it is reeo«--

Sixteen-cell stage viewed front the animal 1>01.-.

(After Surface.) nizable from the first it forms

a landmark by means of

which the cleavage planes of the egg can lie correlated with the
planes of symmetry of the adult.

It is thus found that D is situated on what will be the posterior
side of the embryo in the middle line. The other cells are named
A, B, and 0, following each other round a circle from left to right,
in the same direction as the hands of a clock move when viewed from
above. A and C are situated on the left and right sides respectively

Id

106 INVERTEBRATA CHAP.

whilst B is median and anterior. B and D (in Planocera) are larger
than A and C and meet eacli other in short contact plane at the
vegetative pole, whilst A and C meet each other in a short contact
plane at right angles to this at the upper or animal pole of the egg.

Now the division of these four cells used to he described so that A
was said to hud off a micromere a ; B a micromere b ; and so on.
But this is not a logical description of the event, for the so-called
budding off of a is really the division of A into two cells, a larger
and a smaller, and neither should hear the same name as belonged
to their common mother. So that under an improved nomenclature,
when the four first blastomeres divide, the cells to which they give
rise are denominated la and 1A, ll and IB, Ic and 1C, and Id and
ID respectively ; the smaller letter in each case denoting the
micromere and the larger the macromere (Fig. 80).

When the second group of micromeres is given off, 1A divides
into 2« and 2A, and so on, but to denote the divisions of the already
formed micromeres a different notation is used. Thus la is said to
divide into la1 and la2, where l denotes the daughter nearest the
animal pole, and 2 the one nearest the vegetative pole of the egg
(Fig. 81). When in the 16 -cell stage la1 divides, its daughters
are denoted la11 and la12, on the same principles.

It will easily be seen that this notation is capable of indefinite
expansion. It has, however, one serious defect. Sometimes the two
daughters resulting from the division of a cell lie side by side
at the same distance from both poles of the egg. In this case
1 is held to denote the right-hand daughter, and 2 the left-
hand daughter. But this is confusing, because the eye learns to
associate the symbol '2 with a lower position in the egg than 1,
and it is a strain to grasp the fact that the cell 2a-u may be higher
in the egg than 2«m.

Woltereck in his paper on Polygordius (see Chapter VII.)
gets over this difficulty by using the letters (r} and (/) to denote
right and left instead of the numbers l and 2, if the two daughters
lie to the right and left of the median plane of the egg. Where,
however, they both lie at the side of the egg, then the letters (a)
and (p) for anterior and posterior are employed. This practice
completes the perfection of the nomenclature, but it is unfortunately
not employed by Surface and the other American writers.

Each group of micromeres is known as a quartette, and all the
cells resulting from the divisions of one of the first four blastomeres
are known collectively as a quadrant of the egg.

To return to the special case of Planocera. The cell D is distinguish-
able as the largest of the first four, and, as we have seen, it occupies
what afterwards turns out to be the posterior pole of the embryo.
When once this is recognized the egg is so placed that D is posterior.

In the formation of the first micromeres D divides first, B
follows, and A and C divide simultaneously, so that division takes
place in the order of the size of the cell. The first micromeres

PLATYHELMINTHES

107

are nearly as large as the macromeres, but in the European
genus Discocoelis the inequality in size between micronieres and
macromeres is much more marked. In the next period of cell-
division the second niicromeres are formed by a laeotropic division.

The first quartette divides so as to give rise to two tiers of four
cells, all being of nearly equal size. The lower are of course la2,
Hi1, lc'2, and Id2, and only divide once or twice again.

The third quartette is then formed, and the second quartette
divides, each member giving rise to an upper smaller and a lower
larger cell (2ft2), etc. The cells lal-ldl divide into lower,
somewhat smaller cells, la12, etc., and upper larger cells la11, etc.1
The cells la'2-!^2 divide similarly. When the egg in this stage is

/st quartette

\

2nd
quartette

_ 1st quartette
5A

2nd
quartette

2nd - .
quartette 3D

FIG. 82. — Developing egg of Planocera in<i\dUna. Thirtytwo-cell stage viewed from

vegetative pole. (After Surface.)

viewed from its lower or vegetative pole, the cells belonging
to the second and third quartettes are seen to alternate with one
another and together to form a girdle round the egg just below its
equator (Fig. 82).

After the 32 -cell stage, distinct periods of division, affecting
the cells of the egg simultaneously, cease, and hence the different
groups of cells must be dealt with separately.

An extraordinary feature in Planocera is the formation of the fourth
quartette. In this case Surface still terms the upper daughter a
rnicromere and the lower a macromere, in order to facilitate com-
parison with other eggs of the same type of cleavage. But in
the formation of this quartette the daughter cells, the so-called
"macromeres" (mac, Fig. 84), occupying the vegetative pole of

1 The hyphen between the names of two cells indicates that these names :ire
an abbreviation for the whole quartette. Thus 1al-ldl means 1ft1, 1ft1, lc1, Id1 ; la11,
etc. likewise means the series la11, 1611, lc11, and Id11

108

INVEETEBEATA

CHAP.

the egg, are far smaller than their sister cells, the so-called fourth
quartette of rnicromeres. According to Surface these minute
macromeres are destined to undergo ultimate absorption, and take
no further part in the development. Their nuclei degenerate, the
chromatin in each becoming aggregated into a single deeply-staining
mass ; in fact these degenerating nuclei form an excellent land-
mark by which the egg can lie orientated.

Of the so-called micromeres of the fourth quartette, which are
really the largest cells in the egg, three, viz. 4a, 4&, and 4c, undergo

no further development,
but form masses of yolk
which gradually degenerate
and are absorbed by the
cells of the gut, when this
is formed. The fourth, 4:d,
contains the greater part
of the original macromere
D, and gives rise to the
whole of the endoderm
and a considerable portion
of the so-called mesoderm,
that is, the so-called paren-
chyma or mass of muscular
and connective tissue cells
which intervenes between

FIG. 83. — Optical section of developing egg of Plano-
cera i/n/nili/to viewed from posterior pole. (After
Surface. )

7

mes, the so-called mesodermic bands; N, nuclei of the
three inactive cells, 4a, 4/i, and 4r.

ectoderm and endoderm.

This cell, 4d, divides
into an inner cell termed
by Surface 4^2, and an
outer, 4:dl. (This nomen-
clature is incorrect as 4rf'2 certainly lies above 4<i1.) 4(Z2 divides
into two exactly equal daughters lying right and left of the median
plane of the embryo. Just after this the outer cell, Ad1, divides in
an exactly similar fashion. The inner cells bud off two very small
cells with deep-staining nuclei (end', Fig. 84); they lie just above the
spot where the pharynx will be formed and are incorporated in the
wall of the alimentary canal.

Their larger sisters divide so as to form each a string of cells
directed obliquely forwards on either side (mes, Figs. 84 and 86).
These strings or bands are compared by Surface to the similar bands
which are found in Aimelidan and Molluscan embryos, which arise
from the division of 4rf, and which give rise to the coelorn, but this is
doubtful since the cells in question only occasionally take on a band-
like form. They give rise, according to Surface, to a large portion
of the general parenchyma of the body, but the parenchyma near the
lower pole of the embryo is derived from descendants of cells of the
second quartette, whicli migrate inwards and supply muscles for the
stomodaeum (mes.ect, Figs. 84 and 86) ; this parenchyma is known as

V

PLATYHELMINTHES

109

mes

mesectoderm in order to distinguish it from the parenchyma derived
from 4d'2 which occupies the more dorsal portion of the embryo, and
which is termed mesoderm.

The endoderm, with the exception of the two small cells budded
from 4d2, is all derived from the divisions of 4rf1. This cell, as we
have seen, divides into
right and left sisters ;
each then divides
several times so that
six or eight large cells
are formed, lying at the
posterior pole of the egg
(end, Fig. 84). Soon
afterwards the spreading
edge of the ectoderm,
consisting of the
daughters of the second
and third quartettes of
micromeres, reaches the
lower pole of the egg
and covers this group
of endoderm cells.

During this time the
other three micromeres
of the fourth quartette
have remained un-
divided, but by the
pressure of the daughters
of 4:dl they are pressed
in the egg;

mac

higher

FIG. 84. — Diagrammatic frontal section through egg of
Planocera inquilina at a later stage of development
than that represented in Fig. 83. (After Surface.)

mes, mesodermic bands ; end, endoderm ; einl', small endo
dermal cells formed from mesoderm rudiment; mar, vestigial
macromeres ; mes.cct, cells of ectodermal origin which migrate
inwards to form muscles of the stomodaeum or larval pharynx ;
<7, cells forming rudiment of brain.

up in the

their yolk-granules begin to coalesce so as to form fat-like drops,
and these drops run together so as to form a limited number of
enormous spherules. The nuclei remain large and conspicuous
(N, Fig. 83).

When the ectoderm has completely covered the egg, an invagi-
nation takes place at the lower pole ; this is destined to form the stomo-
daeum of the larva. The four minute "macromeres" become pushed
in before it and ultimately disappear altogether. Then the mass of
cells derived from 4d* begins to separate one cell from another, in the
middle, so as to give rise -to a cavity, the future gut-cavity.

As the endodermic cells multiply they spread in an amoeboid
fashion over the outer surfaces of the yolk-spheres derived from 4",
4&, and 4c, so that these are included within the lumen of the
alimentary canal and are absorbed (Fig. 86). But in J)iM<><-»<'/ix,
according to Lang, 4". and 4ft and 4c bud oil' .small cells which take
part in the formation of the alimentary canal, so that in J'/ti>i»rt'i-«
one member of the quartette does the work which in Discocoelis is
done by all four members. This kind of variation is not uncommon

110

INVEETEBRATA

CHAP.

in eggs with spiral cleavages ; it has been observed both in
Annelida and Mollusca.

We must now return to a more detailed study of the three
ectodermal quartettes. Turning our attention to the first quartette,
we left it at the stage where it consisted of sixteen cells, viz. la11-!^11,
Irt12-ld12, lazl-ld^, and l«22-ld22; la11 is rather larger than
la12, and la21 is larger than la22. lall-ldn bud off four small cells
which occupy the uppermost pole of the egg, these are the so-called
apical cells, l^111-!^111 ; they are little more than nuclei, the
cytoplasm being reduced to a thin plate in which cell limits are
not discernible (ap, Fig. 85).

Now this type of division by which small sisters are separated
at the surface whilst larger sisters remain more deeply situated, is

repeated afterwards by the
larger daughter cells which
have resulted from the division
just described. These cells,
If/.112- Id112, divide each into an
upper very small cell,

and a lower larger cell,
la1122 -Id1122. For the third
time a similar division takes
place. The lower cells resulting
from this last division, 1«1122-
ld1122, give rise to four very
small cells situated externally,
and to four much larger cells
situated internally.

The larger daughter cells
arising from the last division
are denominated l«11221-ld11221.
Once again they undergo a
similar division, each giving
rise to a large internal cell and
a small external one.
Thus we finally get four concentric circles of small cells at the
upper pole of the egg, whilst the four larger internal cells resulting
from the last division form the rudiment of the cerebral ganglion
(g, Fig. 84). The cells, la121- Id121, divide each into two daughter cells
of equal size, but the cells, Ia21-ld21 and 1«22-M-, divide each into a
large internal and a small external cell.

Turning now to the second quartette, each member of course
divided at the time that the third quartette was given off, for until the
32 -cell stage all the cells of the egg divide together. Thus we
have eight cells, 2«1-2(/1 and 2a--2d2 ; if we take the divisions in
quadrant as an example of the whole we find that 2^, divides into a
smaller external cell, la1-, and a larger deeper cell, 2an, whilst 2«-
divides into two equal cells one above the other. The lower of these

FIG. 85. — Developing egg of Planocera inquilina
in a late stage of segmentation, viewed from
animal pole. (After Surface, slightly altered.)

ap, thin apical plate without distinction of cell
outlines formed by the cells «m, feiiij eili, and i/ni.
The dotted lines indicate concentric circles of small
cells near the animal pole of the egg. A third circle
is constituted by the cells composing the apical plate.

V

TLATYHELMINTHES

111

cells lie in the furrows between the large cells of the fourth quartette,
and each of them divides again into two equal cells, the lower of which
'2"'22'2, etc. reaches and touches the corresponding rnacromere, thus
completing the covering of the egg with ectoderm. 2«u, etc. on the
other hand, which had already budded off 2a12 as a smaller external
cell, repeats the process, giving rise to 2«uz externally, and 2^ni
internally. This last cell, 2alu, with the corresponding cells formed

mes

eel

FIG. 86. — Three longitudinal sections through developing embryos of Planoccr/i it

(After Surface.)

Letters as in Fig. 84. In addition, y, yolk spheres resulting from the disintegration of the cells,
4«, 4//, and 4c ; stom, stomodaeum. A, the endoderm forms a solid mass of cells in which the gut-
cavity is just In-winning to appear. B, later stage, the gut-cavity has appeared. C, longitudinal
section of Mailer's larva just after its escape from the egg-capsule.

by the other members of the quartette 2&m, 2cm, 2</ni, give rise
to the mesectoderm, lying at the lower pole of the egg, which almost,
certainly forms the musculature of the stomodaeum which serves as
larval pharynx.

The third quartette of niicromeres undergoes only equal divisions
and all the daughters remain at the surface and are incorporated
in the ectoderm. Beyond this stage Surface could not trace the
ancestry of the cells of the embryo with any certainty.

112

INVERTEBEATA

CHAP.

We have now traced the divisions of the egg to the formation of
an oval embryo, at the lower pole of which is an ectoderinal stomo-
daeum opening above into an irregular endodermic sac lined by small
cells, all trace of the yolky cells of a former stage having disappeared
whilst the upper pole of the egg is occupied by a plate of extremely
small cells, beneath which are ganglion cells.

1

8

FIG. S7. — A, dorsal, and B, ventral views of the free-swimming larva of Yungia. (After Lang. )

1-8, ciliated lobes ; o, month.

Ciliated lobes now appear just below the equator ; there are eight
of these, and from their position they must be formed by the de-
scendants of la'2-lrf2. The larva, which has rotated in the capsule
by the action of these cilia, now escapes and leads a free-swimming
life. It gradually undergoes changes which have not been followed
by Surface in detail, but which Lang has described in Yungia.

METAMORPHOSIS OF THE LARVA OF YUNGIA

Already at the time of its escape from the egg capsule the larva
has lost its primordial radial symmetry. The mouth, which originally

occupied the lower pole of the
embryo, has become shifted on
to one side, which afterwards
turns out to be the ventral side,
owing to inequality in the rate
of growth . of the two sides of
the embryo (Fig. 86, C). Of the
eight ciliated lobes which have
been formed, one overhangs the
mouth, one is mid-dorsal, and six
are lateral, forming three pairs,
the corresponding members of
which are situated to the right
and left of the middle line (Figs.
S7, SS, 89). The band of cilia
which fringes these lobes is continuous from one lobe to another,
so that it forms a continuous girdle surrounding the larva. As the
larva grows older it becomes longer and flatter; eye-spots (oc. Fig.

FIR. 88. — Lateral view of the free-swimming
larva of Yumjin. (After Lang.)

v PLATYHELMINTHES 113

89 B) appear over the region occupied by the apical cells of the

B

6

FIG. 89. — A, dorsal, and B, ventral views of larva of Yiuiyia aurantiaca in which

metamorphosis is Beginning. (After Lang.)

oc, eyespots.

B

6

FKJ. 90. — A, dorsal, and B, ventral views of larva of Ynnijin </ur<i u/i<<< •« in which
metamorphosis is almost complete.

embryo, and the ciliated lobes become less and less prominent
VOL. i i

114

INVEKTEBKATA

CHAP.

(Fig. 90) and finally disappear altogether, so that the larva gradually
becomes transformed into a Polyclade worm.

Of the internal changes which meanwhile take place the most
noteworthy is the formation of the adult pharynx. This arises as a
ring-shaped evagination of the innermost part of the larval stomo-
daeum (stom, Fig. 91), lined by thin cells, from the bottom of which the
pharynx arises as a ridge-like thickening (pli, Fig. 91). During larval
life this evagination is virtually a closed cavity which communicates

1

'/m"

m"x

endanl .* : Ml

FIG. 91. — Median sagittal longitudinal section through larva of Yungia aurantiaca.

(After Lang.)

end, endodermic sac; i-mLaitt, anterior diverticulum of gut passing over brain; li.musc, dorso-
ventral muscles ; y. brain ; 1. in »«•, larval muscles ; ph, rudiment of adult pharynx ; fli , pharynx-sheath ;
stom, stomodaeum or larval pharynx ; rh, rhabdites in ectoderm-cells.

with the stomodaeum by the narrowest slit. As the adult condition
is attained, the outer part of the larval stomodaeum is everted and
its walls become parts of the external surface of the body, the
evagination alluded to above opens widely into the inner portion of
the stomodaeum and becomes the adult pharyngeal sheath surrounding
the pharynx (Fig. 92). During larval life muscles become differentiated
from cells of the parenchyma, and some of these (l.musc, Fig. 91) which
serve to elevate and depress the ciliated processes are of a provisional
character, whereas others (d.musc, Fig. 91) persist as the dorse-ventral
muscles of the adult. The eudodermic sac develops an anterior pouch

PLATYHELMINTHES

115

which projects forwards over the brain (end .ant, Figs. 91 and 92), and
which has been compared by Lang to the so-called excretory canal
of a Ctenophore (v. infra}. The origin of the genital organs was
not observed by Lang. The characteristic rhabdites appear in the
ectoderm cells (rh, Fig. 91) during larval life.

en

J anf

FIG. 92. —Median sagittal section through a young Polyclade worm (Yung ia aurantiaca)
just after its metamorphosis. (After Lang.)

Letters as in pivo'din;; li.-mi'.

THE EVOLUTION OF PLATYHELMINTHES

Now Lang (1889) was led by the study of the European genera
to see a strong resemblance between this type of development and
that of a Ctenophore, and he therefore suggested that Polyclada,
and, inferentially, all Platyhelminthes, are merely Ctenophora which
have become adapted to a creeping form of life.

In Polyclada as in Ctenophora there are large macromeres which
bud off smaller micromeres, and from these last the ectoderm is
formed. In both groups there is an ectodermal stoniodaeuni occupy-
ing the lower pole of the embryo, and at the upper pole we find the
main nervous centre. Further, in both, the primary locomotor organ
consists of eight ciliated ridges of ectoderm, and Lang has shown that
in Miiller's larva the cilia on the ciliated processes are joined edge-
wise so as to form combs. It would perhaps be better to compare the
ascending loops of the ciliated band which intervenes between tw*b of
the larval processes, to the rib of a Ctenophore. Miiller's larva wo
on this hypothesis, represent the pelagic Ctenophore-like ancestor of
Polyclada.

This hypothesis is by far the most plausible that has yet 'been
put forward to account for the extraordinary Platyhelminthes, and it,
is strengthened by the reflection that a creeping Ctenophore, Ctcin>-
plana, exists, in which the alimentary canal is merely lobed, and the
ctenophoral ribs are very much reduced in length ; and by the fact
that a Khabdocoele is known, Monotus, which still, in the adult con-
dition, carries an otocyst above the ganglion, as do Ctenophores.

116 INVEETEBEATA CHAP.

Of course there are differences. Thus there are eight, not four,
macromeres, in Ctenophora, and according to the best account we
have of their development the ectoderm is separated into two sets
of micromeres, not three sets.

But Surface has brought out clearly a hitherto unsuspected
agreement between the two groups, viz. the origin of most of the
so-called niesoderm. This material is really similar in both groups,
consisting of stellate cells with processes, some of which are con-
tractile. In both groups it results principally from cells budded from
the macromeres, after the ectodermal material has been separated off ;
and the small cells budded from the lower poles of the macromeres of
Ctenophora, after they have been almost covered by ectoderm, may
well be compared to the fourth quartette of the Poly clad e.

If we then accept provisionally this theory of Lang's, we are led
to an interesting conclusion. We saw (p. 51) reason to assume the
existence of a free-swimming, blastula-like, ancestral form, of which the
Porifera were concluded to be degenerate sessile descendants. In the
same way, the development of a gastrula from the blastula was shown
to be evidence that the whole group of the Coelenterata are descend-
ants of this pelagic group. Of this pelagic group, when it had attained
the Coelenterate stage of development, the greater portion, as we saw in
the last chapter, took to a sessile life, but one portion, the ancestors
of modern Ctenophora, retained their free-swimming life. We now
conclude that from this group of what we may term primitive
Ctenophora, a set of degenerate descendants arose which gave rise to
the Platyhelminthes.

The history of the Metazoa, so far as we have yet traced it, is that
of a main pelagic group increasing in complexity of structure as time
goes on, and at each level throwing off creeping and sessile stocks
which are more or less degenerate in structure. We have indicated
that the Polyclada are the only group of Platyhelminthes from the
study of whose development much light can be expected on the origin
of the phylum ; but our knowledge is extremely defective even of the
development of the Polyclada.

The student here meets with a phenomenon which will recur
throughout the course of his study of Invertebrate Embryology, and
it is this, that while the early development of the egg up to the
period when the embryo becomes free, is known with some accuracy,
next to nothing is known of the larval and post-larval stages.
The reason for this ignorance lies chiefly in the difficulty found in
obtaining appropriate food for the larva when the embryonic stores
of nourishment are exhausted. This difficulty has been overcome in
the case of Echinodermata, and further study will, no doubt, enable
us to overcome it for the other groups also.

As a consequence of this state of affairs, however, there are vast
gaps in our knowledge of the development of every group of Inverte-
brates ; these gaps can and should be filled up. They offer a most
promising field for further work. Thus, for example, in the develop-

v PLATYHELMINTHES 117

merit of Polyclada, we desire to know the origin of the extraordinary
excretory system which is so characteristic of Platyhelminthes and,
so far as we know, entirely unrepresented in any Ctenophore ; also a
knowledge of the development of the genital cells and of the genital
ducts would be of extreme interest.

On the subject of the development of the excretory system Lang
has a few observations. He has observed two ectoderniic ingrowths
at the sides of the embryo anteriorly, and these he looks upon as the
rudiments of the main excretory canals ; but we ought to have a
detailed knowledge of their development.

When the development of Polyclada is thoroughly known the
embryonic development of the other groups of Platyhelminthes will
become of greatly increased interest, for it will show what alterations
in a known type are produced by access to stores of food, and in this
way throw light on the laws of variation, the ascertaining of which
constitutes one of the root problems of the Science of Biology.

LITERATURE REFERRED TO

Keeble and Gamble. The Origin and Nature of the Green Cells of Convolula
roscoff'e nsis. Quart. Journ. Micr. Sci., vol. 57, 1907.

Lang. Die Polyclaclen des Golfes von Neapel. Fauna and Flora des Golfes von
Neapel, vol. 11, 1889.

Surface. The Early Development of a Polyclad Planocera inquilina. Proc. Acad.
Nat. Sci. Philadelphia, 1907.

CHAPTER VI
NEMEETINEA

Classification adopted

Protonemertini
Mesonemertini
Metanemertini
Heteronemertini

THE group of worms known as the Nemertinea constitute a very
interesting division of the animal kingdom. They nsed to be re-
garded as a subdivision of Platyhelminthes, with the more primitive
members of which they agree in possessing a soft ciliated skin. They
also agree with Platyhelminthes in the character of their excretory
system and in the general structure of their nervous system, but they
differ profoundly from all Platyhelminthes in possessing an anus.
The acquisition of a second opening to the alimentary canal and the
consequent separation of the functions of ingestion and egestion, or
defalcation, is a great structural advance, and is a reason for regarding
Nemertinea as standing on a much higher level than Platyhelminthes.
The Nemertinea are divided by Burger (1895) into four groups,
Protonemertini, Mesonemertini, Metanemertini, and Heteronemertini.
The development of the members of the first two divisions is quite
unknown. Metanemertini pass through a shortened development
within the egcr-shell, the details of which have not been worked out

oo

owing to the extremely minute size of the eggs. The majority, how-
ever, of Heteronemertini develop into a free-swimming larva which,
after leading a free life in the sea for some time, undergoes a re-
markable metamorphosis into the adult worm. There are two types
of this larva known, one termed the Pilidium and the other the larva
of Desor. But the larva of Desor is quite evidently a simplified
form of Pilidium, modified for a creeping rather than for a swimming
life, and the Pilidium must be looked upon as the typical larva of the
group.

CEREBRATULUS LACTEUS

We select therefore for special description the American species
Cerebratulus lacteus, the eggs of which develop into a typical Pilidium.

Joo^

118

CHAT". VI

NEMERTINEA

119

The development has been worked out by C. B. Wilson (1900), and
later by E. B. Wilson (1903), but similar species exist in the
Mediterranean with very similar development, and have been worked
at by E. B. Wilson's pupils, Yatsu (1904) and Zeleny (1904).

The egg of Cerebratulus lacteus whilst still in the ovary has a
loose glassy membrane which at one end is drawn out into a point
and thus offers a landmark in the egg ; after the egg has been laid
the spindle for the formation of the first polar body is formed, and
this causes a little protuberance at the opposite pole of the egg.
Unless fertilization supervenes the spindle is never completed, but
when fertilization takes place the first and then the second polar
bodies are nipped off and the loose glassy membrane is dissolved.

The egg divides into four macromeres so exactly similar to one

Fit;. 93. — Two stages in the segmentation of the egg of Cerebratulus lacteus viewed
from the side. (After E. Wilson. )

71, polar bodies. A, 16-cell stage. B, 28-cell stage passing into 3'2-cell stage.

another that it is quite impossible to distinguish an A, a B, a C,
and a I) segment, consequently the naming of the quadrants in the
segmenting .egg is an arbitrary matter. From these four macromeres
quartettes of micromeres are budded off" — the first quartette dexio-
tropically, the second laeotropically, until no less than six quartettes
have been formed (Fig. 93).

The exact fate of these quartettes is not described in detail by
Wilson. He remarks, however, that the endoderm extends to the
equator of the spherical embryo. From this we infer that, as usual,
the upper or ectodermic half of the segmented egg is constituted by
the three first quartettes of micromeres ; and that the fourth, fifth,
and sixth quartettes, together with the residual maeromeres, con-
stitute the endoderm. The residual macromeres are similar in
size and appearance to the last quartette of micromeres.

In this way a hollow sphere of cells, the blastula, is formed which
is uniformly ciliated. Then one side of it becomes flattened and the

120

INVERTEBEATA

CHAP.

mes.ect

cells here are somewhat larger than elsewhere. The whole shape of
the blastula now resembled an obtuse cone.

Two large cells are budded into the cavity of the blastula, or
blastocoele, one at each side of the flattened surface. These attach
themselves by pseudopodia to various portions of the blastula wall.
Then a patch of cells lying in the centre of the flattened surface is
invaginated and forms a sac-like gut, whilst at the apex of the cone
a thickening is formed which becomes slightly invaginated and forms
a saucer -shaped depression. The cells forming this depression

develop long stiff cilia, and in this
way a characteristic apical sense-
organ is formed. The blastula has
thus become a gastrula (Fig. 94).

Each of the two large colls which
passed into the blastocoele divides so
as to give rise to a mass of branched
cells, and these cells put out long
pseudopodia which attach them-
selves to gut, to apical organ, and to
skin, and some of these pseudopodia
become converted into muscle fibres.
Such cells are termed mesenchyme.
The gut becomes differentiated into
a sac -like globular stomach and a
funnel-like oesophagus.

Round the edge of the flattened
surface there is differentiated a
thickened band of cells carrying
specially long cilia. This band is

called the " prototroch," and it becomes the sole locomotor organ of
the embryo, which now becomes a larva, escaping from the egg-shell
and swimming about. The shell is broken by a spiral boring move-
ment executed by the embryo. The prototroch is at first a simple
circle, but it grows out into two lateral, downwardly -directed
processes, like the ear-lappets of a policeman's helmet, and so the
characteristic form of the Pilidium larva is attained (Fig. 95).

The principal muscles which have now been formed by the mesen-
chyme are as follows : — The retractor of the apical plate is a band
of fibres which is attached above to the apical plate, and passes down-
wards splitting into right and left portions. These latter fibres are
at first attached to the gut, but later, when the lappets are formed,
they extend down into them, and their muscle fibrils extend from the
oesophagus to the stomach, and from the post-oral ectoderm to the
stomach ; there is a strong sphincter muscle round the mouth.
These muscles are all formed by processes of the larger mesenchyme
cells. The smaller mesenchyme cells apply themselves to the inner
surface of the ectoderm and to the outer surface of the gut. -They
give rise to a series of so-called " peritoneal " muscles which take the

FIG. 94. — The young gastrula of Cere-
bratulus lacteus. (After C. Wilson.)

«/), apical plate; end, gut; mes.ect, mother
cell of mesenchyme.

VI

NEMEKTINEA

121

form of a fenestratecl sheet. In the lappets the peritoneal muscles form
radial muscles which serve to contract and elevate the lappets (Fig. 9G).

B

mes

OC '

. ^m&mmtimmw?'^ "v;-mtmam

'Ifjprv

FIG. 95. — Two stages in the development of the Piliclium larva of Cerebratuhis lacteus.
Showing the development of mesenchyme into muscles. A, Earlier stage. B, Later
stage. (After C. Wilson.)

/, lappets of prototroch ; oe, oesophagus ; nt, stomach. Other letters as before.

fniiscper

FIG. 96. — Two views of advanced Pilidium larva of Cerebratulus lacteus to show Ihr

development of the muscles. (After Wilson. )

A, viewed as a transparent object. B, surface view, am, anterior amniotic invagination ;
musc.per, so-called peritoneal muscles ; ret, retractor of the apical plate.

On the posterior wall of the oesophagus a groove for conducting
food appears, and numerous gland cells appear all over its wall.

122

INVERTEBRATA

CHAP.

Running round the edge of the larva under the prototroch a nerve-
ring has been detected.

The development of the Pilidiuni is now complete, and it swims
about at the surface of the sea feeding on microscopic organisms
which are whisked into its mouth by the action of its cilia. After

.jar

aim.

FIG. 97.— A Pilidium larva shortly before its metamorphosis. (After Metschnikoff.)

Letters as before. In addition, a.im, anterior imaginal disc ; e.s, rudiment of cephalic slit ;
in; rudiment of proboscis ; p.im, posterior imaginal disc ; oes, oesophagus.

about two weeks it begins its metamorphosis. This has been described
by Metschnikoff (1869) and Salensky (1886).

On the flattened under side four ciliated imaginations of the
ectoderm are formed. These are termed the amniotic invaginations,
and their deeper portions are the imaginal discs. Two of these
invaginations are situated opposite one another on the right and left
sides of the animal respectively, in front of the mouth, and . two
others are similarly situated behind the mouth. Each of them grows
and deepens, extending upwards over the surface of the globular

VI

NEMEKTINEA

123

stomach. Finally they meet one another, fuse and coalesce, the
anterior and posterior on each side and the right and left on each
side. The imaginal discs form the skin of the future worm whilst
the outer walls of the coalesced imaginations form a temporary
envelope known as the amnion.

Before coalescence is quite complete the organs of the future worm
are constructed, and as to the manner in which this is accomplished
we have tantalizingiy little information. It appears from Salensky's
account (1886) that the skin of the anterior part of the animal, as far
back as the cephalic slits, originates from the anterior imaginal discs.
The posterior imaginal discs form the skin of the hinder part of the
body of the worm. The characteristic proboscis is formed as an
ectodermal invaginatiou. The proboscis sheath originates as a solid

p.im

JT I

aim

oes

FIG. 98. — Longitudinal section through a Pilidium larva of about the age of that
represented in Fig. 97. (After Salensky.)

Iir, rudiment of brain ; sh, rudiment of sheath of proboscis.

mass of mesoderm into which the proboscis invagination projects
(Fig. 99). This mesoderm appears to be in close proximity to the
ectodermal wall of the posterior imaginal disc on each side and
possibly arises from it. Later the rudiment of the sheath becomes
hollowed out and forms a sac lined by flattened cells and filled with
fluid. The adult brain (br, Fig. 99) arises as a thickening of the
ectoderm of the anterior imaginal discs. The cephalic slits likewise
arise as ectodermal ingrowths, not from the imaginal discs but from
the larval ectoderm between anterior and posterior discs, and pouches
grow out from the oesophagus to meet them (oe.p, Fig. 99 A). An anus
must be formed, but as to how or when we have no information.

In fact nearly all our information about this period of development
is based on the examination, as whole objects, of larvae fished from the
sea, although Salensky has to some extent applied the method of
sections. If once an appropriate food for the Pilidium larvae could be

124

INVERTEBEATA

CHAP.

discovered, so that these larvae could be reared in large numbers
through their metamorphosis, under experimental conditions, and if
each stage in this change were thoroughly examined by sections, then
a Hood of much-needed light would be thrown 011 this period of
Nemertine development.

If the reader has followed the description so far given it will be
evident that when all four amniotic invaginations completely coalesce
they must cut the larva into an upper and a lower half. This is just
what happens ; and the lower and inner half, invested by the coalesced
floors of the amniotic invaginations, and containing the alimentary
canal, drops to the bottom of the sea and commences life as a young

pr

aim

-p.im

FIG. 99. — Two stages in the development of the Nemertine rudiment within the Pilidiuni,

viewed from above. (After Salensky.)

c.s, cephalic slits ; o, mouth ; oes.p, oesophageal pockets.

Nemertine worm. The upper half consisting of the larval ectoderm,
including the prototroch, lappets, and apical sense organ, and bounded
inside by the coalesced roofs of the invaginations or amniotic invest-
ment, continues to swim about for a little time before its energies are
exhausted, and then it dies.

EXPERIMENTAL WORK.

E. B. Wilson and his pupils Yatsu and Zeleny have performed a
most interesting series of experiments on the eggs and embryos of
Cerebratulus, the general results of which may be shortly recounted
here. The unfertilized egg was cut or shaken into fragments. If
this be done before the membrane of the nucleus has disappeared, and
if sperm be added to the fragments, only the fragment in which the

vi NEMERTINEA 125

nucleus is situated develops into a larva. But if the same experiment
be performed after the nuclear membrane has faded, all the fragments
will develop into larvae. It is, therefore, obvious, that when the
nuclear membrane fades, some substance must pass into the cytoplasm
which confers on any fragment of it the power to develop into a larva
if a spermatozoon be added to it.

If the same experiment be performed after normal fertilization
has occurred, only the fragment containing the first invading
spermatozoon will develop. All attempts to fertilize the other
fragments by adding fresh spermatozoa failed.

In the majority of cases the developing fragment is the one
containing the zygote nucleus ; but in some cases, when the frag-
mentation of the egg had occurred before the spermatozoon had reached
the nucleus, it is the fragment containing the spermatozoon and
not that containing the nucleus which develops, while the fragment
containing the latter can be seen to form the polar bodies, but it goes
no farther in development.

Therefore, just as some substance must exude from the egg nucleus
which confers on all the cytoplasm the power to form a larva, so we
are bound to conclude that some material is given off from the sperm
head which inhibits development in the cytoplasm, except when under
the influence of the first nucleus.

When the egg was cut into fragments, however, and a piece was
induced to develop, it gave rise to a perfect Pilidium larva of
correspondingly reduced size. The segmentation occurred as in the
normal larva, though the blastomeres were correspondingly smaller.
But when the first two blastomeres of a normal egg were separated
from one another, each divided as if it still formed part of the whole
egg, — it formed two macromeres and two micromeres. The separation
was effected by exposing the developing eggs to the influence of
artificial sea- water, made up so as to entirely exclude lime ; such
water causes the blastomeres to lose their adhesion to one another
and to fall apart, owing apparently to an alteration in the physical
characteristics of the outermost layer of the cytoplasm. The separated
blastomeres are then restored to normal sea- water and allowed to
continue their development.

When one of the first four blastomeres is separated it forms one
macromere and one micromere by the first division, and continues to
segment as if it formed one-fourth of the egg. Nevertheless in both
these cases the half or quarter blastula closes its wound by narrowing
and contraction of the edges, and develops into a Pilidium which is
perfectly normal but of reduced size. The Pilidium which develops
from one of the first four blastomeres, however, has its apical plate
displaced forwards, a change which is probably due to the size of the
cells, derived from the segmentation of the blastomeres, remaining the
same as if they still formed part of a whole egg. Each cell has
therefore to form a part of the larva proportionally four times as great
as it would normally have done, and so it must be subjected to

126 INVERTEBRATA CHAP.

much more severe curvature than usual, and these curvatures produce
a series of strains which distort the resulting larva.

A cell of the 8-cell stage is incapable of developing into a
Pilidium. When the 8-cell stage is broken in two, its two constituent
portions, viz. the macromeres and the first quartette of micromeres,
each group of four cells can develop into a larva. But the micromeric
group form a larva with a very large apical sense-organ and no gut,
whilst the macromeric group develops into a larva with an enormous
gut and no apical organ. The same result is obtained by cutting the
blastula along the equator, in this case the upper half forms a larva
with enormous apical organ and vestigial gut, whilst the lower half
forms a larva with large gut and no apical organ. Hence we conclude
that whereas every one of the first four blastomeres contains all the
substances necessary to form a perfect larva, after the occurrence of
the third cleavage the substance necessary for the formation of the
gut is restricted to the lower cells, whilst that destined to form the
apical organ is confined to the upper four cells.

Yatsu found that when the fertilized egg is cut into fragments
abnormal Pilidia are produced, except where only a small fragment
from the animal pole has been removed, and hence he concludes that
the material destined to form the apical plate is situated not at the
animal pole but in a ring a short distance beneath it.

When we review the results of these experiments we are struck
with the demonstration which they afford of the influence of the
materials given off from the nuclei on the cytoplasm, and also with
the proof that at the moment when sperm and egg nuclei approach
one another a definite structure or arrangement of organogenetic
materials is impressed on the cytoplasm. The outward and visible
sign of this inward process may be the radiations which extend from
the sperm nucleus outwards. This conclusion will be supported by
evidence to which we shall call attention during our study of various
other invertebrate groups. The structure impressed on the cytoplasm
reminds us of what \vas found to be the case with the Ctenophore egg,
but it is not so definitely specialized as in the Ctenophore egg. In
this respect the egg of the Nemertine occupies an intermediate
position between the egg of the Hydromedusan and the egg of the
Ctenophore.

AFFINITIES OF NEMERTINEA.

We now approach the final question as to what light the develop-
ment of Cerebratulus throws on the ancestry of the Nemertinea as a
whole. This question resolves itself into the problem : What is the
ancestral significance of the Pilidium larva ? We have to interpret a
larva with a simple sac-like gut, opening by a mouth at its lower pole,
whilst its upper pole is occupied by a cup-like sense-organ carrying
long stiff cilia, and its locomotion is effected by a lobed band of cilia.
Just as in the case of Mliller's larva we are again reminded of a
primitive Ctenophore. Mliller's larva does not carry the apical tuft

vi NEMERTINEA 127

of hairs, and in this respect is less like a Ctenophore than the Pilidium
larva ; but in having its ciliated band produced into eight processes
instead of two, it is more like a Ctenophore than the Pilidium. We
probably shall not go far. astray in concluding that the Pilidium
represents a free-swimming ancestor of the Nemertinea, belonging to
the same great group as that containing the ancestor of the
Ctenophores, but differing from the latter as a shark differs from a
salmon, whilst both are fish.

The metamorphosis into the Nemertine worm must be regarded
as the immensely shortened recapitulation of the long development
which occurred before this ancestor developed into a Nemertine ; a
development which must have been much longer than that which
was necessary to convert the ancestor denoted by Miiller's larva into
the Polyclade worm. Proof will be given as our studies proceed, that
such a cataclysmic metamorphosis as that of the Nemertine has been
secondarily derived from a type of development that was originally slow
and gradual. Nevertheless, as we have indicated above, if this meta-
morphosis were thoroughly studied in detail we should know a great
deal more about the steps by which that change was accomplished
than we do at present.

LITERATURE REFERRED TO

Burger. Die Nemertinen. Fauna n. Flora des Golfes von Neapel, vol. 22, 1895.

Metschnikoff. Studien iiber die Entwicklung der Ecliinodermon und Nemertinen.
Mem. Acad. St. Petersb., series 7, vol. 14, 1869.

Salensky. Bau und Metamorphose des Pilidium. Zeit. fur wiss. Zool., vol. 43,
1886.

Wilson, C. B. The Habit and Early Development of Ccrebratulus ladeus. Quart.
Journ. Mier. Sci., vol. 43, 1900.

Wilson. E. B. Experiments on Cleavage and Localization in the Nemertine Egg.
Arch. Ent-Mech., vol. 16, 1903.

Yatsu. Experiments on the Development of Egg Fragments in Cerebratulus. Biol.
Bull., vol. 6, 1904.

Zeleny. Experiments on the Localization of Developmental Factors in the Nemertine
Egg. Journ. Exp. Zool., vol. 1, 1904.

CHAPTER VII

ANNELIDA

Classification adopted

Archiannelida

Chaetopoda

Polychaeta

fNereidiformia
Spioniformia
Terebelliformia
Capitelliformia
Scoleciformia
Scabelliformia

.Hermelliformia

.Oligochaeta

fAcanthobdellidae
Hirudinea - Rhyncobdellidae
[ Gnathobdellidae

THE group of segmented worms known as Annelida has furnished
subjects for an immense amount of embryological study, but
there are a great many points in their development still unsettled
which offer a wide field for future research. Although widely diverse
from each other in their adult structure the members of the group
show a remarkable uniformity in their early development, so that
the complete description of a single type will serve as a guide to
what is known about the development of all.

Annelida are divided into Archiannelida, including Polygordius
and a few allied forms which never develop chaetae and are devoid
of external circular muscles ; Polychaeta, the central group, including
worms with numerous chaetae, well-developed parapodia, and external
circular muscles ; Oligochaeta, freshwater and terrestrial worms, with
few chaetae, complicated genital organs, no parapodia, but provided
with external circular muscles ; and Hirudinea, extremely modified
forms with obscure segmentation, no chaetae or parapodia, but with
external circular muscles, extremely complicated genital organs, and
suckers used for progression.

( )f these forms the most primitive, and the one which shows the
longest larval development, is the Archiannelidan Polygordius. The

128

CHAP, vii ANNELIDA 129

embryology of this form has been worked out in great detail recently
by Woltereck (1902, 1903, 1905), and we select it as type for special
description. As, however, although Polyyordius occurs on both sides
of the Atlantic and in both North Sea and Mediterranean, it is not
very abundant or easy to obtain, some practical directions will be
given as to the means of dealing with the eggs of Pomatoceros, a very
common Polychaete belonging to the family Serpulidae. The develop-
•ment of Pomatoceros, in the early stages at least, is almost identical
with that of Polygordius, and in one or two points even more primitive.
The eggs of all Annelida undergo cleavage of the spiral type,
which we have already studied in the case of the Platyhelminth
Planocera. In Annelida, as in Planocera, the ectoderm is separated
as three successive quartettes of micromeres. As in Planocera also,
a blastula consisting of relatively few cells is formed, which, by
invagination or epibole (see p. 92) is converted into a gastrula.

METHODS

Now for the study of such eggs the method of sections is of very
little use. This method requires that the egg to be studied should
consist of a large number of similar cells, so that a sample such
as a section presents would give a good idea of the whole ; but
where the egg consists of relatively few cells and these are in-
dividualized at an early stage of development the method obviously
fails. So there is nothing left but to make whole mounts and
endeavour (as Surface did in the case of Planocera) to identify and
trace the history of each individual blastomere.

This procedure, as already mentioned (Chap. V. p. 10-i), is termed
the study of Cell-lineage ; it was introduced by the American
zoologist Whitman (1878), who first employed it in the study of the
eggs of Hirudinea, and it was taken up by a brilliant school, which
Whitman founded, one of the most prominent of which was Prof.
E. B. Wilson (1892).

Prof. Wilson applied the method to the study of the development
of. the Polychaete Nereis, a work which threw much light on
Annelidan embryology. Other pieces of work of equal merit were
those of Tread well on Podarke (1901) and Child on Arenicola (1910).

If, nevertheless, we select the work of a German for special
description, when the credit of most of the investigations belongs to
Americans, it is solely because the development of the type on which
he worked is so primitive and simple that, once it is known, all the
others can easily be described in terms of it.

In order that the cells may be identified in whole mounts of eggs,
it is necessary that these should be rendered transparent, and that
they should be examined from all sides. As the eggs of many species
are opaque owing to the fact that they contain numerous yolk grains,
this is not easy to do. Prof. E. B. Wilson employs a mixture of 3
parts of glacial acetic acid and 1 part glycerine. This mixture
in many eggs dissolves the yolk granules and makes the whole of a

VOL. I K

130

INVERTEBKATA

CHAP.

glassy transparency. The preparations made in this way, however,
are not permanent, but they last long enough to enable good draw-
ings to be made. Other authors make permanent preparations by
preserving the eggs in "Eisig's mixture," i.e. 3 parts of saturated
aqueous solution of corrosive sublimate and 1 part of glacial acetic
acid, staining with haematoxylin and trusting, after dehydration by
alcohol, to oil of cloves to clear them sufficiently to allow of complete
examination.

In order to examine the eggs from all sides Wilson rolls them
about on the slide by moving the coverslip, which he supports 011 feet

made of a mixture of
beeswax and vaseline, the
proper height of which
can be ascertained by
trial. Other workers
attain the same end by
introducing between
slide and coverslip a piece
of thin capillary glass rod
or tube, drawn out to
the requisite degree of
tenuity.

When the segmenta-
tion is completed the
embryo issues from the
egg membrane and com-
mences to lead a free
life as a larva. The form
of this larva resembles
in broad outline the form
of the Pilidium. Like
it, it possesses an apical
plate with a tuft of long-
cilia and a prototrochal
girdle, and it is called a
Trochophore.

The Trochophore
differs from the Pilidium
in possessing an intestine
terminating in an anus,
and in having a post-
trochal region of the body which projects behind the prototroch,
instead of having only a concave surface in this position such as is
found in the Pilidium. By the gradual growth and elongation of the
post-trochal region, the body of the worm is formed.

In the case of the Serpulid Pomatoceros the eggs and sperm are
easily obtained by simply extracting the animals from their tubes and
placing them in clean sea-water. If the genital cells are ripe they

int

AN.

mtir

FIG. 100. — The Trochophore Larva of Polygordius,
viewed from the side. (After Woltereck. )

A.N, archinephridium ; ap, apical plate ; int, intestine
nit.tr, inrtatroch ; o, mouth; p.tr, prototroch; st, stomach
t.tr, tetotroch.

viz ANNELIDA 131

will immediately be shed, and in this way a natural fertilization of
the eggs is accomplished.

The Trochophore issues on the second day and rises to the top of the
water. It can be reared through its entire development by supplying
it with a pure culture of the diatom Nitscliia. Such pure cultures
can be obtained from Dr. Allen, Director of the Marine Biological
Station at Plymouth, and they serve as pabulum for many different
kinds of larvae.

Pure diatom cultures were obtained originally by isolating under
the microscope a single individual of the species of diatom desired,
and then transferring it to a llask of sterilized and filtered sea- water.
The sea-water is first shaken up with animal charcoal and decanted
in order to remove all soluble toxins, and then passed through a
Berkfeldt stone filter, which removes all organisms, even bacteria.
To the sea-water is now added a certain amount of Miguel's solution,
about 2 drops per 100 c.c. of water, and the flask is stopped by a plug
of sterilized cotton wool. In a month's time a copious growth of the
desired diatom is obtained.

If a pipette-full of such a culture be added to an evaporating dish
containing the larvae of Pomatoceros, these will develop normally
and eventually metamorphose into the adult worms, which form
tubes and attach themselves to the sides of the glass. In this way
the whole life-cycle can be controlled, and such larvae can be
examined living, or mounted whole, or examined by sections.

The fixative found best is Eisig's mixture (see ante). The methods
of orientating, embedding, and cutting have been fully described
in Chapter II.

POLYGORDIUS. CELL-LINEAGE

Returning now to Polygordius we should remind the student that
this is a minute worm which burrows in mud and sand. The eggs are
excessively minute and very transparent, and the segmentation is
remarkable for its extreme regularity. The eggs are dehisced into the
sea by the breaking up of the parent's body and are fertilized there.

Up to the 64-cell stage all the cells divide at the same time, so
that we have successive " cleavages " which successively divide the egg
into 2, 4, 8, 16, 32, and 64 cells, that, is six cleavages in all. More-
over a 128-cell stage is very nearly realized, for all the cells of the
04-cell stage divide nearly synchronously, except those forming
the prototroch and a few others of the upper hemisphere, which,
having reached the summit of their development, divide no more.
The macromeres are all precisely equal in size ; it is therefore at first
impossible to discriminate an A from a B, a 0, or a D (see Chapter V.),
but in the later cleavage stages this can be done, owing to the different
way in which members of the second and third quartettes of
micromeres, given off from the different macromeres, behave.

Shortly after the 64-cell stage has been reached cilia appear
on the cells destined to form the prototroch (Fig. 101, B). The

132

INVERTEBEATA

CHAP.

embryo then begins to rotate within the vitelline membrane, which
it soon ruptures, and it then begins its free-swimming existence.

112

mac

mac

mac

FIG. 101. — Stages in development of the blastula of I'<>l)i<j(>nUus seen in optical

longitudinal section.

A, 32-cell stage ; B, 64-cell stage ; C, T<5-cull stage ; D, 116-cell stage. Letters as before. In
addition, mar., residual macromeres ; p, polar bodies ; v, \acuoles in cells forming the prototroch ; rit,
vitelline membrane ; l<ym, the apical cells ; 1-7112, the mother cells of the Annelidan cross.

When about 140 cells have been formed the fully-segmented egg
constitutes a thick-walled, extremely flattened blastula which is con-

vn ANNELIDA 133

verted into a gastrula, and then into a Trochophore, by rearrange-
ments of cells, without further cell-division. Further divisions of
cells only occur after the Trochophore has been feeding for some
time.

Up to the 64-cell stage then, all the cells of the egg divide
simultaneously, so that the first mieromeres divide once as the second
quartette of mieromeres is given off. When the division to form the
third quartette of mieromeres is complete, the first quartette have
divided twice ; and when the fourth quartette, which gives rise to
mesoderm and endoderm, is formed, they have divided thrice, and with
this division the 64-cell stage is attained.

The egg, which from the 16-cell stage had taken on the form of
a hollow spherical blastula, now begins to flatten out. In the same
period the second quartette of mieromeres has divided twice and the
third quartette once.

At the next cleavage the cells of the prototroch fail to divide
and so do certain other cells, descendants of the first group of
mieromeres, but all the other cells of the egg divide. A fifth
quartette is given off, which is destined to form endoderm only, and
the residual macromeres are now barely if at all larger than the
mieromeres to which they gave rise. The flattening of the embryo
continues till it assumes the form of a flattened plate (Fig. 101, 1)).

The next cleavage is participated in only by the macromeres,
which divide not spirally but symmetrically with regard to the future
median plane of the embryo. The fifth quartette of mieromeres also
divide, so do the fourth, and some cells of the second and third ; and
then invagination commences.

In describing in detail the divisions of the cells it is most
convenient to deal with the different quartettes of mieromeres
separately. Since, as has been already stated, it is impossible in the
earlier divisions to distinguish one macromere from another, it is
convenient to be able to refer to them collectively, and the letter q is
used to denote a, b, c, and d.

In all four quadrants of the egg the divisions of the first
quartette of mieromeres are exactly alike. We say that lq divides
into upper cells lq1, mothers of the whole upper hemisphere of
the Trochophore above the prototroch, and into lower cells lq2,
the mothers of the prototroch ; lq1 divides again into upper cells
lq11, mothers of. the .apical plate, or as it is sometimes termed the
rosette, and of a St. Andrew's cross of cells radiating from it, called
the " Annelidan cross " because it is conspicuous in the eggs of all
Annelids ; and into lower cells lq12, mothers of a group of cells called
by Wilson the intermediate girdle cells but termed by other authors
the Molluscan cross, because in Molluscan eggs these cells take on
the form of a conspicuous upright cross, lq'2 divides into l<i"', ;iml
lq22, one set of cells lying obliquely above the other.

At the next cleavage Iq11 divides into lq111, forming the apical
cells or rosette which carry the tuft of long stiff cilia which con-

134

INVEETEBEATA

CHAP.

stitutes the apical sense-organ, and into lq112, which form the rudi-
ment of the Annelidan cross, lq112 bud off cells between them-
selves and the apical cells, and in this way the arms of the cross
are formed, that is to say, lq112 divide into lq1121 and lq1122.

Turning now to the other cells of the upper hemisphere we find
that lq12 behaves similarly. It divides into lq121 and lq122, and
lq121 further divides into .lq1211 and lq1212. These three cells in
each quadrant, lq122, lq1212, and lq1211, are in four curved series, and
this is also true of primitive Mollusca, but in higher Mollusca they
are arranged in four straight lines and form the upright cross
mentioned above.

112

Ill

FIG. 102.— Dorsal view of upper hemisphere of egg of Polygordius, in which seventy-six

cells have been formed.

The rosette cells and the cells of the prototroch are left clear. The cells of the " Molluscan " cross
are cross-hatched. Those of the " Annelidan " cross are marked with circles.

The group of cells lq21 and lq22 each divide into two sets of cells,
so that we have four daughters of lq2 in each quadrant ; and these
sixteen cells acquire long powerful cilia and constitute the prototroch.
They become large, clear, and vacuolated, and at first — and this is
most interesting and important — they form four discrete groups ; it
is only later that these groups coalesce to form a complete ring.

If this description lias been followed it will be seen that the upper
hemisphere of the egg, including the prototroch, when divisions
temporarily cease, consists of forty cells. In the 04-cell stage it
consists of course of thirty-two cells, since it forms exactly half
the egg, but the cells constituting the "Annelidan" and "Molluscan"
crosses divide once again, and this brings the total number of cells
up to forty.

vii ANNELIDA 135

When we turn the flattened embryo over and view it from the
vegetative pole, we are able, once the 64-cell f stage has been
passed, to distinguish the various quadrants of the egg from one
another, and to tell which is A and which is B, which C and which D.

Now the embryo has a somewhat squarish outline and the
rounded corners are formed by the groups of prototrochal cells
belonging to the first quartette. These groups are directly opposite
the respective macromeres from which they arose ; for, if \ve take
the group derived from A for example, all its members are daughters
of la2 and ultimately of la. But la itself was given off dexiotropically
from A ; that is to say, lay above and to the right of it. The next
division is a laeotropic one, that is to say, as the name implies, la1,
the upper daughter, lies above and to the left of the lower daughter
la2. Now this formation of the spindle with a left bend has the
effect of causing la2 itself to pass somewhat to the left, and thus
undo to a certain extent its original right-hand twist, so that it
eventually comes almost exactly opposite A.

The line joining the prototrochal group of cells and the
macromeres constitutes a radius of the figure, and cells or cell groups
lying on this radius are said to be radial, and cells or cell groups
alternating with them are said to be inter-radial. Now it is found
that the third and fifth quartettes of micromeres are radial whereas
the second and fourth are inter-radial. The following rule then is
found to hold for the fate of cells forming these quartettes. In the
radial quartettes the cells in quadrants A and B behave alike, but
the cells in C and D \vhile behaving like each other behave differently
from those in A and B. In the inter-radial quartettes the cells in
quadrants in A, B, and C, behave alike, but the cells in quadrant D
behave differently from each of them.

Turning our attention now to the second quartette, and taking a
as example for a, b, etc., we find that 2a divides into 2ax and 2a2,
one directly above the other. Each then divides laeotropically into
2an and 2a12, and 2a21 and 2a22, respectively, thus forming a lozenge-
shaped group of four cells. Of these four the outermost divides
radially into 2alu and 2a112, lying almost side by side ; whilst 2a12
and 2a21 divide obliquely into 2a121 and 2a122, 2a211 and 2a212
respectively. These cells help to form a belt of flat clear cells lying
just beneath the prototroch, and they divide no more till the
Trochophore stage is reached. The fate of the innermost cell 2a22
is different ; it divides by a tangential cleavage into an outer cell
2a221 and an inner cell 2a222. Then each of these divides into a larger
anterior cell 2a221n and 2a'222a respectively and a small posterior cell
2a221P and 2a222P respectively.

Exactly the same division takes place in quadrant C, and then the
small posterior cells sink into the blastocoele and form that part of
the mesectoderm or larval mesoderm, which will eventually give
rise to the circular an/l radiating muscles of the larval oesophagus.

In quadrant B, however, 2b'-"21 divides into an outer and upper

136

INVERTEBKATA

CHAP.

cell 2b2211, and an inner and lower cell 2b2212 whilst 2l>222 divides into
two sisters lying side by side, viz. 2b222r and 2b2221. Now these four
cells in quadrant I>, and the two cells in quadrant A, viz. 2a221a and

2€

Fio. 103. — (Continued on opposite page.]

2a222a, and in quadrant C, viz. 2c221a and 2c222a (Fig. 103, C), are destined
to form the stomodaeum, Itut for the complete history of this
structure we must wait until we have considered the history of the
third quartette of micromeres.

VII

ANNELIDA

137

In the quadrant D the divisions at this stage are similar, but
2d22'2 and 2d'2il do not divide until the Trochophore stage is reached. It
follows that the so-called larval mesoderm is formed from the second
quartette in three of the four quadrants of the egg.

We now pass to the consideration of the third quartette, and we
would remind our readers that this quartette is radially situated,
whereas the one we have just been considering was inter-radial ; and

spp

FIG. 103 (continued}. — Three stages in the segmentation of the lower or vegetative surface

of the egg of Polygonlins.

A, stage of about 76 cells ; B, stage of about 112 cells ; C, later stage in which a mass of rapidly
dividing cells at the lower pole is sharply distinguished from an outer zone of clear cells. The heavy
black line surrounds the cells which later will take part in the process of invagination and the
formation of the lips of the blastopore. The cells belonging to the second quartette are dotted,
those belonging to the third quartette are marked by vertical lines. The cells belonging to the
fourth quartette are marked by little circles, those belonging to the fifth quartette by horizonlM
lines. The residual macronieres, and those belonging to the first quartette, are left white. The names
of the cells which form the larval mesoderm are surrounded by circles. Cf. ('Ja^'p).

further, as in eggs with spiral cleavage in general, the second and
third quartettes of micromeres come to lie about the same parallel of
latitude, so to speak, on the globe represented by the whole egg, since
the quadrants of one quartette occupy the gaps between the
quadrants of the other.

Taking then the quadrant A first (and what applies to A is true also
of B) we find that 3a divides into 3a: and 3a2; and each of these now
divides into an anterior and posterior cell, i.e. 3a];i, -"'a'1', 3a'2a and
3a2P, respectively. Of these the first two 3ala and 3alp, remain

138 INVERTEBRATA CHAP.

undivided and help to complete the belt of broad flat cells, the other
parts of which are formed by the cells of the second quartette, to
which allusion has already been made. The other two cells each
divide into an anterior outer large cell, 3a'2al and 3a2P1, respectively,
and a posterior inner smaller cell, 3a2a2 and 3a2P2, respectively. The
last two eventually sink into the blastocoele and help, like the
similar cells of the second quartette, to form larval mesoderm, whilst
their two larger sisters enter into the formation of the stomodaeum.

We are now able to take a more general survey of the cells which
enter into the formation of this structure. The front wall of the
stomodaeum is formed by the four cells 2b2211, 2b2212, 2b222r and 2b2221.
Its right side is constituted by the cells 2c'221a and 2c222a, and its left
side by the corresponding cells 2a221a and 2a222P. In its right anterior
corner we find the cells 3b2al and Sb2?1, in its left anterior corner the
corresponding cells 3a2al and 3a2pl.

In the quadrants C and D the micromeres of the third quartette
divide, at first, similarly to those belonging to quadrant A, B. Thus,
taking 3d for example (and remembering that all said about it is equally
true of 3c), we find that it divides into 3d1 and 3d2, and each divides
into anterior and posterior cells : of these 3dla and 3d1? become broad
and flat and remain undivided, and thus complete the band of this
kind of cell right round the egg ; though at a later period, as we shall
see, they form part of the posterior lip of the mouth. 3d2a divides
into 3d2al and 3d'2a2, and these cells will help to complete the hinder
wall of the stomodaeum in a manner to be described later. 3d2'3,
however, divides into an anterior and a posterior cell, 3d2?a and 3d2PP,
and both these cells undergo another similar division, so that we get
an antero-posterior directed line of four cells, 3d2paa, 3d2PaP, 3d2PPa, and
3cl2PPP (Fig. 103, C).

The last two of these cells constitute the rudiment of one of
the larval kidneys or archinephridia, the other being formed by the
corresponding cells in quadrant C. The more anterior cell of each
pair at a later stage sinks into the blastocoele and is transformed
into a flame cell or solenocyte, with a cavity and a tuft of cilia
waving within it ; whereas 3d2pPP forms the excretory tube and
remains in connection with the ectoderm (Fig. 10G).

Passing now to the foiirth quartette we find that all four cells
divide radially, each giving rise to two daughters lying side by side ;
so that we have 4aa and 4a?, 4br and 4b', 4ca and 4cP, and 4dr and
4d', as we pass round the egg. Of these all but 4dr and 4d' enter
into the formation of the gut wall : the last named will eventually
give rise to those longitudinal streaks of cells known as the
mesodermic or germinal bands. These bands will eventually
become hollowed out to form the coelom or true body-cavity, the
walls of which constitute the adult mesoderm.

The fifth quartette divides also at first evenly, 5a into Sa1 and
5a2, 5b into Sb1 and 5b2, 5c into 5c* and 5c2, and 5d into Sd1 and 5d2.
In quadrants A and B the division stops, but it goes on in quadrants

vii ANNELIDA 139

C and D ; in these 5cl and 5c2 divide into 5cn and 5c12, and into 5c21
and 5c22, respectively ; and the same thing happens to 5d] and 5d2.

This greater growth in the hinder quadrants of the egg, which
occurs both in the 3rd and 5th quartettes, has the effect of pressing
the pairs of cells Sa1 and 5a2, and 5bl and 5b2, out of their original
arrangement of two lines converging to the lower vegetative pole of the
egg, into a position of two lines parallel to one another, and they will
eventually form the sides of the mid-gut (Fig. 106).

The residual macromeres 5A, 5B, 5C, and 5D, lastly divide, each
into two equal daughters ; 50 and 5A into anterior and posterior cells,
5B into right and left cells by radial divisions ; but 5D divides into
an inner and an outer cell 5D1 and 5D2, and the outer 5D1 divides
again into 5D11 and 5D12, so that here, as in the fifth quartette, we
have increased multiplication of cells in the hinder part of the egg.

These divisions complete all the divisions of cells which take
place in the flattened plate-like blastula. We have, as we have
already seen, 40 cells of the first quartette. Of the second we have
8 stomodeal, 4 larval mesoderm, and 26 cells forming the belt of
flattened cells ; i.e. 38 in all. Of the third quartette 8 enter into
the formation of the stomodaeum, and 4 form larval mesoderm, 4 form
larval kidneys, and 4 form ventral ectoderm (3c2paa and 3cpap, + 3d2paa
and 3d2pap, respectively), making 28 in all. The fourth quartette
contains only 8 cells, the fifth 12, and there are 9 residual
macromeres. So that the grand total of all the cells at this stage is,
40 + 38 + 28 + 8 + 12 + 9 ; i.e. 135 in all.

At this point of development imagination of the cells of the
lower surface begins, and the blastula is converted into a gastrula
which, in virtue of its apical plate and its four groups of prototrochal
cells, may be already termed a Trochophore.

We shall now study how imagination is brought about. The
nine residual macromeres form a plate at the vegetative pole. The
two cells forming the centre of this plate, namely 5D2 and 5D12, rise
upwards into the blastocoele, in consequence no doubt of altered
chemical conditions here, that is, of altered cytotaxis. As the
centre of the plate thus sinks in, two lateral ridges of cells become
prominent and outline the edges of the indentation so formed ; in a
word they outline the blastopore. These lateral ridges are, on the
right side, ob1, 5b2, 4ca, 5c12, and 5cn ; on the left side 5a\ oa2, 4aa
5d12 and 5dn.

The blastopore takes on the form of an oval opening, elongated
in an antero-posterior direction. The front of the blastopore is formed
by the cells 4br and 4b', and the hinder end at this stage by the cells
4dr and 4d'. The centre cell in each row (4aa and 4ca) approaches its
opposite partner and so the ridge of the oval is converted into a
figure of eight. These two latter cells finally meet one another and
the oval opening is thus cut into two openings, the primitive mouth
and the primitive anus respectively.

The primitive mouth persists, but the primitive anus is temporarily

140 INVEETEBEATA CHAP, vn

closed by the union of the four cells 5c12, 5cl12, 5cu, and Sd1
respectively. At a later period of development, however, the
permanent anus re-opens at the same spot, so that the temporary
closure is an event of no importance.

We have thus the problem solved before our eyes hoiv, out of a
single primitive opening used both for injestion and egestion or defaeca-
tion, such as we find in Coelenterata and Platylielmintlies, separate
openings for injestion and egestion were formed.

When the primitive anus is closed the blind end of the gut
remains in close contact with the cells 4dr and 4cV. Two outer
columns of cells parallel to the first two are then formed. These
consist on the right side of 2c222a, 2c222P, 3c2a2, and 3c2Paa, and on the
left side of 2a222a, 2a222P, 3d2a2, and 3d2Paa. The hinder cells of these
two outer ridges also meet; i.e. first 3c2a2 and 3d2a2, then 2a222P and 3c222P,
and lastly 3c2paa and 3d2Paa ; but their front cells, 2c222a and 2a222a, do
not meet ; they, as we have already seen, help to form the sides of
the stomodaeum (Fig. 104, B).

As these outer columns of ectodermal cells meet, the endodermic
pouch shrinks away from them and leaves a blastocoelic space
between it and them ; so that the process of closing the ventral wall
of the gut is completed before the ventral ectoderm is complete, and
thus, for a brief moment, the blastocoele is actually in open com-
munication with the external world (Fig. 105, C).

The final closing of the outer part of the blastopore is effected
by the rotation inwards and backwards of the cells 3c'2Paa and 3d2Paa.
These cells rotate through an angle of 180°, and so come to lie actually
within and behind the cells 3c2PaP and 3d2PaP (Fig. 104, I)).

It is at this stage of development that the cells 3c2PPa and
3d2ppa Wander like amoebocytes into the blastocoele and form the
solenocytes of the two archinephridia. The pre-anal tuft of cilia,
the telotroch, is formed by the cell 3d2Paa. The lower lip of the large
mouth is formed by the cells 3cla, 3dla, 3c2al, 3d2al, 3c2a2, 3d2a2, which
swing through a right angle to occupy that position. The cells 3clp,
3dlp, become elongated in an antero-posterior direction, acquire short
cilia, and form the metatroch, i.e. the circular band of feebler cilia,
which runs parallel to the prototroch behind the mouth (Fig. 104, D).

Turning our attention now to the second quartette in quadrant
D, we find that the cell 2d222 wanders like an amoeba over the ventral
surface of 4dr and 4dl Each of these cells has by this time budded
off a small anterior cell, 4drl and 4d'\ which is the beginning of the
adult mesoderm on each side.

We find now, when we look at the under side of the Trochophore
behind the mouth, two large thin plate-like cells 3c2pap and 3d'2pap in
front. These constitute what Woltereck calls the hyposphere, or
under surface of the almost spherical larva. To the sides of these,
lie 3c2pPp and 3d2pPp, the tubal cells of the archinephridia. Behind
them are a group of three compact cells covering the adult mesoderm ;
and these cells which, for reasons to be explained later, we call the

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142

INVEETEBEATA

CHAP.

B

trunk blastema, are

3c2Paa, 3d2Paa, and 2d222.
Outside and behind
these are thin plate-like
cells, belonging to the
quadrant D of the
second quartette, but
immediately behind
them lie the cells 2d212
and 2d221, which mark
the point at which,
about this time, the
anus is re-formed.

Proceeding now to
examine the cells which
enter into the gut-wall,
we find that the ven-
tral surface of the
gut is formed (1) by
the union of the pair
4aa and 4ca which, as
we have seen, by join-
ing with one another,
cut the original blasto-
pore into two openings ;
and (2) by the union of
the following pairs of
cells belonging to the
fifth quartette, viz. 5d12
and oc12, 5dn and 5cn,
and at a slightly later
period, the pair 5d21 and
5c21, which also unite
with one another.

As the dorsal wall
of the gut is invaginated
the Trochophore swells
out and becomes arched
dorsally, recovering in
this way from its

FIG. 105. — Four diagrammatic transverse sections of lower flattened slianp Thp
part of young Trochophore larva to show mode of ,. .

closure of blastopore. (After Woltereck.) cells which form the

A, gastrulation beginning ; B, constriction of blastopore, the dorsal Wall, irOlll being

cells of fourth quartette approach one another ; C, inner lips of Cubical become flattened

blastopore closed ; D, outer lips of blastopore closed. The Qj}(J COllVCl'ted illto thill
ligures refer to the quartettes to which the cells thus designated ,

belong. M, residual macromeres. ai'Clied Shells OI CytO-

plasm. The front wall
of the mid -gut where it joins the stomodaeum is formed by the

VII

ANNELIDA

143

cells 4b' and 4br, which, it will be remembered, were originally
situated at the front rim of the long oval blastopore. (Jells Sa1
and So1 also form part of the front wall of the mid-gut, being situated
below 4b' and 4br. The lateral walls of the mid-gut are formed on
the left by 5B1 above, by 5a2, in the middle, and 4aa below ; and on
the right by the corresponding cells 5Br, 5c2, and 4ca.

The hinder wall of the mid-gut, where it joins the intestine, is
formed on the left by 5Aa, on the right by 5Ca, and in the mid-dorsal
line by 5D'2. The valve which projects into the cavity of the gut

oes ret.

FIG. 106. — Optical sagittal section of young Trocliophore after gastrulation is complete.

(After Woltereek.)

Letters as in preceding figures. In addition, V, intestinal valve (this is represented in outline) ;
oes.ret, larval retractor muscle of oesophagus.

and tends to separate the cavity of the mid-gut from that of the
intestine, is formed by the following pairs of cells, one member of each
pair being situated on the right side and the other on the left, — 4cP
and 4aP, 5B? and 5C?, 5c22 and 5d22 ; and in addition by 5D12 in the
mid-dorsal line.

The intestinal wall is formed by three pairs of cells, 5c12 5cn and
5c21 on the right, and 5d12, 5dn, and 5d21 on the left side, and by
the single cell 5D11 in the mid-dorsal line. Its hinder wall is
formed by 4d12, 4dr~, which at this period form part of the gut wall
but which later are the mother cells of the adult mesoderm.
Between and slightly behind them, a little later, the permanent
anus arises, and since they formed the hinder rim of the original

144 INVEETEBRATA CHAP.

blastopore and later of the primitive anus, it will be seen that the
permanent anus corresponds to the hindermost piece of the primi-
tive one.

The Trochophore is now complete and can begin to feed. It is
the only larva in which the ancestry of every cell has been
completely worked out, and hence its cell-lineage has been given with
a completeness which it will not be necessary to repeat in the case of
other forms. As now constituted it is very similar to the Pilidium, for
the ventral surface is still almost flat and no trace of the projection
which is to form the body of the future worm, has yet appeared. It
is true that the Pilidium possesses no anus, but this, as we have seen,
is also true of the young Trochophore.

The distinctive features of the Trochophore at this stage are the
metatroch, the archinephridia, and the telotroch, all of which are
wanting in the Pilidium.

FURTHER DEVELOPMENT OF POLYGORDIUS

There are two species or varieties of the European Polygordius,
one found in the North Sea, P. lactens, and one in the Mediterranean,
P. appendiculatus. The segmentation of the egg and the early
development up to the attainment of the Trochophore stage is
strikingly similar in both varieties, but the later development, till
the attainment of the adult form, is very different in the two cases.
The adult worms according to Woltereck are practically indistinguish-
able from each other, so that we have here a curious instance
of specific peculiarities being developed during the later larval
history.

We shall describe the later development of the Neapolitan species
first, as it is the simplest. The external features of this stage of
development were exhaustively described by Fraipont (1887), but its
true significance has only been made clear by Woltereck (1902 and
1905). In this species, after feeding has gone on for some time, a
rapid period of cell division and growth sets in in the three cells
forming the trunk blastema (these it will be remembered are 2d~
and 3c2paa and 3d2Paa) ; and in two cells, 4drp and 4dlp, the mother cells
of the adult mesoderm which lie internal to the three cells just men-
tioned. These two latter cells had already, in the Trochophore, each
budded off a small cell (4drl and 4dn) in front of them : this process
is now repeated many times, and in this way two long strings of
cells, the mesodermic bands, are formed. The original mother cells
of the bands are termed teloblasts.

The multiplication of the cells of the trunk blastema furnishes
new ectoderm to cover these bands, and in this way a post-trochal
outgrowth of the body is formed. The intestine elongates at the
same time by the growth and division of the cells forming its walls,
for the anus is situated at the termination of this post-trochal
projection.

VII

ANNELIDA

145

By longitudinal divisions the mesodermic bands become several
rows of cells thick, and a faint indication of the division of the post-
trochal " body " into segments is now discernible. These segments
are indicated in the ectoderm by faint transverse grooves parallel to
one another; in the mesodermic bands by the appearance in each
band of a set of cavities, which we may term somites, situated
one behind the other, corresponding to the grooves in such a
way that, in each segment,
one pair of cavities is formed.
The right and left somites in
each segment rapidly expand
and displace the blasto-
coele, and finally meet one
another both above and below
the intestine. Then, where their
walls impinge on one another,
absorption takes place, and so
instead of two coelomic sacs one
coelomic ring-shaped space is
found in each somite.

Whilst these changes have
been taking place the archine-
phridia have undergone further
development, by the adhesion to
them of further cells budded
from the third quartette. The
original pore cell divides and
gives rise to a string of cells.
The original name cell, or soleno-
cyte, persists, but the newly-
added cells form additional
solenocytes. The transformed

oes

PN

ttr

nephridia are now known as the
first pair of protonephridia
(P.N1, Fig. 108, A). Each consists
of a tube which forks internally
into two branches, and eacli

FKI. 107. — Later stage in the development of
Polygordius appendiculatus, in which the
" worm-body " is being formed by the
growth of the trunk blastema. (After
Woltereck. )

Letters as before. In addition, «, permanent
anus; li.li, hind limit of head blastema; int, intes-
tpnn Pdinrwnnf nli'ir tine '< P-N> protonephridimn ; oes, oesophagus ; st,

immates in two peculiai 8tomach . <A frout limit of trullk blastema,
solenocytes. Each of these

solenocytes consists of a head studded all over with blind cuticular
tubes, each of which contains a flagellum (sol1, Fig. 108, A). Behind
this pair of protonephridia a second pair arises. Each of these
consists of a tube opening by a pore on one side in the region of
the first somite formed from the trunk blastema. The tube is
terminated internally by solenocytes which are situated in the
swollen body of the Trochophore, and which are derived from
wandering cells, descendants probably of the third quartette. The
tube itself owes its origin to a pore cell situated in the ectoderm of

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CHAP, vii ANNELIDA 147

the trunk blastema; this cell buds so as to form a string of cells, which
become hollowed out so as to constitute a tube.

Further cell multiplication has also been proceeding in the region
of the rosette or " Annelidan cross," around the apical plate, and this
region of new-formed cells is termed the head blastema. On each
side, just as in Planocera (see page 110), cells are budded inwards
into the blastocoele and form the rudiments of the larval cerebral
ganglion. Other cells of the larval mesenchyme form muscular
strands which reach from the apical plate to the sides of the
oesophagus and to the ventral ectoderm in front.

As the post-trochal outgrowth of the body increases in length its
tissues begin to undergo histological differentiation, but unfortunately
the details of this have not yet been worked out in Polygordius. As
more and more somites are formed we can make out, in the most
anterior and advanced somites, the longitudinal muscles. These
appear to be laid down as hard refractive fibrillae in the basal
portions of the cells forming the outer wall of the coelorn ; the visceral
muscles also make their appearance as similar fibrillae in the basal
parts of the cells forming the inner wall of the coelom.

The origin of the posterior or permanent nephridia, the meta-
nephridia, as we may term them, has not been fully worked out.
Woltereck asserts that they arise as strings of cells, growing from
" pore-cells " situated in the ectoderm of the trunk blastema. At an
early stage of their development they appear as small packets of cells
lying in the outer wall of the coelom, where the insertion of the
oblique septum separates dorsal and ventral bundles of longitudinal
muscles. In the adult, as is well known, the inner ends of these
nephridia communicate with the coelom by ciliated funnels. How
these are formed has not been made out in Polygordius.

The origin of nephridia in Annelida generally has been the
subject of much dispute, but a great deal of light has been thrown on
this subject by the results of investigations on the development of
the Oligochaete worm Criodrilus, details of which will be given later.

The head blastema undergoes important changes as the larva
grows older. We have already seen that underneath the apical tuft
of cilia there is formed a mass of nerve cells and nerve fibres, which
constitute the larval cerebral ganglion. From this ganglion there
proceeds eight radial nerves which go to the cells forming the
prototroch. Two of these, termed lateral nerves, are stronger than
the rest ; these cross the prototroch and join the ectoderm cells which
will give rise to the ventral nerve cord of the adult. They con-
stitute the nerve collar of the adult. Of the six other radial nerves,
two are situated on the anterior side of the larva, whilst four are on
the posterior side.

Besides these radial nerves there is a network of ganglion cells
and fibres underlying the ectoderm of the upper half of the larva,
and, though in a much sparser condition, beneath a good deal of the
ectoderm of the lower half. There is also a ring of nerve fibres

148 INVEKTEBKATA CHAP.

underlying the prototroch, and another underlying the metatroch.
Apparently the radial nerves do not communicate with the plexus,
and in this respect the Trochophore resembles a Ctenophore, for there
is in the adult Ctenophore a plexus of nerve fibres under the
ectoderm which is quite distinct from the radial bands which underlie
the " ribs."

As the larva grows the apical ciliated cells fall off and the spot
where they existed becomes a pit, soon overgrown from the sides by
thickenings of the ectoderm. These lateral masses (probably derived
from the Annelidan cross) form short thick pits from whose bases the
head tentacles arise (t, Fig. 108). The ganglion, however, persists
for some time, but it is soon overshadowed by two lateral masses of
nuclei which constitute the rudiment of the paired supra-oesophageal
ganglion of the adult. These masses lie beneath and to the outer
sides of the rudiments of the tentacles ; they probably arise from the
inner parts of the lateral arms of the " Molluscan " cross ; they enter
into connection with the two lateral nerves which ultimately form
the nerve collar of the adult. Behind the tentacle bases there appear
two shallow grooves : these acquire, later, stiff cilia and become the
ciliated pits (c.p, Fig. 108) of the adult. At the extreme outer
edges of the head blastema there appear two small pits lined by
pigmented cells. These are the eyes of the larva.

Underneath the lateral nerves the lateral muscles are formed
later by the accumulation of mesenchyme cells. These connect with
the trunk blastema and persist, though they do not become
functional until the metamorphosis. A mid-dorsal muscle is formed
in the same way and is not functional during the larval period.

These sub-epithelial muscles which are taken over into the adult,
are not to be confounded with purely larval muscles, mentioned above,
which traverse the blastocoele. These transitory larval muscles are,
(1) a pair of oesophageal retractors running from the head blastema
to the skin just above the mouth (oes.ret, Fig. 106); (2) a pair of
main retractors running from the head blastema underneath the
origin of the tentacles to the trunk blastema (ret, Fig. 108, B) ; (3)
a pair of dorsal "elevators" (elv, Fig. 112) arising from the dorsal
surface half-way between the apical plate and the prototroch ring,
and running downward to join the trunk blastema ; (4) a plexus
of muscle fibres underlying the skin everywhere and crossing each
other in various directions ; and (5) two powerful ring muscles, one
underlying the prototroch and one the metatroch.

Before the growth of the post-oral segmented region is quite
complete, the intermediate girdle cells intervening between the
region of the prototroch and the " head blastema," gradually degenerate
and disappear. They pass from a flattened to a columnar form,
their nuclei are dissolved, they assume a glassy appearance and then
are cut off either internally, when their remains are devoured by
amoebocytes, or externally ; and so the head blastema comes into
contact with the prototroch ring on its upper margin. A few of

VII

ANNELIDA

149

these intermediate cells, however, just at the margin of the head
blastema, become transformed into gland cells (gl, Fig. 109), which
are almost certainly of an excretory nature.

A similar contact takes place between the lower end of the
prototrochal ring and the front end of the new ectoderm, forming
the trunk blastema (arising chiefly from the descendants of the cell
2d222); so that the cells forming the hyposphere (descendants of
3c2Pap anc{ 3cj2pap) j-,ave &\so been absorbed.

The larval oesophagus gradually loses its cellular walls, which are

musc.L

x to show

FIG. 109. — Two sections of the anterior part of ,1 larva of Polygonl ! H s

the changes supervening on metamorphosis. (After Woltereck.)

A, frontal section just before, metamorphosis. B, sagittal section just after mrtamnri>li'>sis.
Letters as before. In addition, c.f, ciliated filter ; gl, excretory gland cells. The coclomic cavities c.r
the somites are dotted but the blastocoele has a pale uniform tint.

replaced by new cells budded from two lateral pockets. These
pockets may be compared to the "imaginal discs" of insects (see p.
267). The renewed oesophagus is delimited from the stomach by a
ring of ciliated cells. From the walls of the stomach, cells are given
off into its cavity and degenerate, and in this way the globular
stomach slowly decreases in size. The boundary separating .sinm.-ieh
from intestine is, of course, marked by a projecting valve. This is
armed with stiff cilia so as to constitute a ciliated filter (c.f, Fig. 1 09).
When the growth of the post-oral region has reached its full
extent cataclysmal changes take place. The circular muscles under-
lying the prototroch contract so vigorously as to cut the skin uniting

150 INVERTEBRATA CHAP.

the edges of the head and trunk blastemas and of the prototroch. The
oesophageal and main retractors, and the three sub-epithelial muscles,
contract and pull the head blastema down until it is in contact with
the upper end of the trunk blastema. The prototroch is cast off as a
crumpled collar.

The globular stomach is to a large extent dragged back into the
trunk by the peristaltic swallowing action of the visceral muscles,
which are not closely adherent to the gut wall. The sphincter
separating the end-gut from the stomach closes ; the remains of
the stomach are then broken up and devoured by phagocytes and
the renewed oesophagus comes into contact with the end-gut. Thus
the intestine is again completed.

The retractors of the oesophagus and the main retractor and
elevator muscles are broken through by the intense contraction,
and absorbed, but the sub-epithelial muscles persist and become
continuous with the ventral and dorsal longitudinal musculature of
the adult.

The first pair of protonephridia break up and disappear, and so

FIG. 110. — Polygordius neapolitanus immediately after metamorphosis.

(After Woltereck.)

Letters as before. In addition, Ti.b, hinder limit of head blastema ; t.h, frontal limit of trunk blastema.

do the heads of the second pair of nephridia, but the U-shaped
tube of each of these persists as a nephridium of the first segment
or peristomium.

The two coelomic sacs which are contained in the peristomial
segment, diverge in front, and between their dorsal ends a section of the
blastocoele projects backwards and becomes continuous with the
dorsal and ventral blood-vessels ; the vessels themselves indeed are
but the spaces between right and left sacs in successive segments.
The lining of these blood-vessels is provided by free wandering
amoebocytes which apply themselves to their walls (mes, Fig. 111).

Immediately after the metamorphosis brain and pharynx are in
close contact, and the blastocoele in this neighbourhood is squeezed
out, but later a space between them again develops, which we
may term the schizocoele (schiz, Fig. 111). The pharynx be-
comes surrounded by a thick mantle of cells derived from the
descendants of 3a2 and .">b2, and this mantle becomes split into an
inner and outer layer. From the latter are derived radiating1
muscles ; these are inserted at one end in the ectoderm, while in
the other direction they traverse the space between inner and outer
layers and insert themselves in the oesophageal cells. The inner

VII

ANNELIDA

151

layer become nerve cells, whence nerve fibres run along the pharynx
in a longitudinal direction (oes.m, Fig. Ill, A).

When the animal has stripped off its prototroch it sinks to the
bottom : the eye-pits become functional, but their principal use is to
avoid the light. When eventually the adult adopts a burrowing life
the eyes generally degenerate.

In the North Sea species, P. lacteus, the later development is
somewhat different from that which we have just described. Thus, a

vr-

vtv-

FIG. 111. — Longitudinal sections of anterior portion of Polygordius nenpolitfiniis immediately
after metamorphosis, to show details. (After Woltereck.)

A, frontal section at level of oesophagus and intestine. B, frontal section dorsal to intestine. C,
sagittal section. Letters as before. In addition, W, dorsal blood-vessel ; oes.m, mantle of ectoderm
cells surrounding oesophagus; schiz, schizocoelic space in front of brain; 6.r, blood ring; r.7, ventral
blood-vessel ; we.*, wandering cells in the blastocoele.

ring-shaped invagination of the thin ventral surface of the larva is
formed, giving rise to a circular fold, which we shall term the
amniotic fold, surrounding the trunk blastema; and the space between
this fold and the ectoderm covering the trunk blastema — in a word,
the cavity of the invagination — grows forwards and upwards in the
form of four pockets, a dorsal, a ventral, and two lateral.

When further growth and cell division begin in the trunk
blastema the new post-trochal body thus formed is folded up within
the cavity covered by the circular fold just mentioned, and only at
the moment of metamorphosis is the body straightened and thrust

152

INVEKTEBEATA

CHAP.

forth as the segmented trunk of the adult worm. Previous to this
period it is held in its compressed and crumpled condition, alonp- its
surface to its posterior end, by extensions of the main blastocoelic
retractor and elevator muscles. When these break through during
the ^ intense contraction which accompanies metamorphosis, the
straightening process begins.

A further difference between the two species of Polygordius is
found in the condition of the nephridia. In P. lacteus the archi-
nephridia remain small and unbranched, and the only change which
they undergo in becoming converted into the first pair of proto-
nephridia is to become covered with numerous cuticular tubes — each

am/

PN.

PN

*fr an.

FIG. 112. — Late larva of Polygordius lacteus in optical frontal section. (After Woltereck.)
Letters as before. In addition, am.f, amniotic fold ; elv, larval elevator muscle ; t.fr, telotroch.

containing a flagellum — so as to resemble, in fact, one of the soleno-
cytes of the first pair of protonephridia of Polygordius appendiculatus.
The second pair of protonephridia take the form of long tubes studded
all over with solenocytes, which are directed dorso-ventrally, parallel
with the prototroch, and which open dorsally at the beginning of the
post-trochal region.

It is obvious that the development of P. lacteus as compared with
that of P. appendiculatus is shortened and modified. In some points
indeed it reminds us of the development and metamorphosis of the
Pilidium larva of the Nemertinea. Thus we could compare the four
amniotic invaginations of the Pilidium larva to the four pockets
which arise from the circular groove in the Trochophore, since in
both cases the adult body is formed from their inner walls ; but the

vii ANNELIDA 153

rilidium differs radically from the Trochophore in the fact that its
apical plate is cut off with the rest of the larval skin, whereas in the
Trochophore larva it persists and forms part of the covering of the
adult head.

EEMAINING ANNELIDA

A great number of other species of Annelida have been worked at,
chiefly Polychaeta, but in no single case with anything like the
thoroughness with which Woltereck has worked out Polyyordius.
The Oligochaeta and Hirudinea have no free - swimming larvae.
Their eggs are laid enclosed in cocoons along with a milky nutritive
secretion, and within these they pursue their development until they
attain the adult form ; so that, as one might expect, the development
is profoundly modified as compared with the Trochophore of Poly-
gordius, nevertheless in broad outlines the same general course of
development can be discovered.

POLYCHAETA

Turning our attention now to the Polychaeta we find that the
first important point to be borne in mind is that a true Trochophore
larva is found in very few cases. In most cases the rapid develop-
ment of the ectodermal descendants of 2d2, which in Polyyordius
marks the conclusion of the Trochophore stage, begins long before the
embryo escapes from the egg membrane ; so that when it does escape
it has the form of a post-trochophoral stage with several somites
already developed (Fig. 116).

In a word the development of such worms is, as compared with
that of Polyyordius, " telescoped." This is true of Nereis among
Nereidiformia, Capitella among Capitelliformia, Arenicola among
Scolecifonnia, and Amphitrite among Terebelliformia. In other
cases, such as Sternaspis, the endoderrn consists of large yolky
cells, and neither mouth nor anus is developed when the larva
begins its free existence.

It was formerly customary to classify Annelidan larvae by their
ciliated bands. Such classification is obsolete, but we shall give
the significance of the terms as they are still used by some.
Atrochal larvae are those in which there is an apical tuft
of cilia and a general ciliated covering, but no prototroch.
Such is Sternaspis ; of course they are degenerate forms. Monotro-
chal larvae with prototroch only, are the early stages in the typical
development of the Trochophore ; they become later telotrochal—
by the development of the telotroch as described in Polygordius.
Mesotrochal larvae, such as that of Capitella, are forms where the
metatroch only is developed, the prototroch being undeveloped.
Polytrochal larvae are really post-trochophoral stages in which
accessory hoops of cilia are developed on the worm's body to assist in
locomotion (Fig. 116).

154

INVEETEBRATA

CHAP.

As we have already hinted, however, in many of the Sabelliformia
there is a development closely resembling that of Polygordius, and
the animal begins its larval life as a true Trochophore. In the genus
Eupomatus, according to Shearer (1911), the blastopore divides into
primitive mouth and primitive anus — as in Polygordius the mouth
opening persists but the primitive anus is closed ; later the permanent
anus is formed just where the primitive anus disappeared. In
this form, when the Trochophore has begun to swim about, there is
as yet no trace of adult mesoderm; the mother cells of this layer
4dr and 4d' are still situated in the wall of the intestine, and only
when the larva has been leading a free-swimming life for a day or

end

-an.v

M 'lft.tr

FIG. 113. — Figure illustrating the origin of the mother cells of the adult mesoderm in

Kiijiamtifiix. (After Shearer.)

A, section of young gastrnla showing the inward migration of endodenn cells and the formation of
the mother cell of the mesoderm by the division of one of them. B, sagittal section of Trochophore
larva three days old. C. sagittal section of hinder end of Trochophore larva, much enlarged, ou.r,
anal vesicle; ap, apical plate; end, endoderm ; M, mother cell of mesoderm lying in endoderm ; p.tr,
prototroch ; P.N, protonephridium ; .-.•?, stomach ; t.tr, telotroch.

two do these cells emerge from the gut wall and begin to found the
mesoderm bands. Further, in Eupomatus, the two archinephridia,-
which are formed exactly as in Polygordius by the migration inwards
of certain cells of the third quartette and which develop so as to
form the only pair of protonephridia present in this larva, persist in
the adult, and here constitute the two large effective nepluidia
which serve as principal excretory organs ; they are situated in the
prostomium and open by a dorsal pore. According to Shearer they
open near the anus in the larva, but their opening becomes shifted by
the growth of the " worm-body." The Trochophore of Eupomatus is
further remarkable for developing a large clear vacuole, the so-called
anal vesicle (an.v, Figs. 11.'! and 114), in the cells which support
the telotroch.

VII

ANNELIDA

155

In the two following points, namely, the primitive situation of the

mother cells of the meso-

derm in the wall of the

gut, and the persistence

of the protonephridia,

Eupomatus can fairly

claim to show, on the

whole, a more primitive

development than even

Polygordius. A detailed

study of the develop-
ment of this form, or of

that of the allied genus

Pomatoceros, is greatly

to be desired.

Turning now to

Nereis as an example of

the " telescoped " form

of development, de-
scribed in detail by

Wilson (1892), the first

difference that strikes

us as compared with

Polygordius is that the

macromere D is, from

the first, distinguishable

from the other three

by its greater size. The first quartette of micromeres are, however,

equal in size and their development is,
in broad terms, the same as in Poly-
gordins. In each quadrant, however,
one of the trochoblasts does not develop
cilia, but joins the intermediate girdle
cells to form part of the covering of the
upper hemisphere.

When,however,the second quartette
of micromeres are given off, the pos-
terior one, 2d, called by Wilson " the
first somatoblast," is very much larger
than its sisters, and after a few pre-
liminary divisions proceeds to bud oil'
ventral plate of ectoderm cells

)

FIG. 114. — Diagrammatic saggital section of fully-grown
Trochophore larva of Eupomatus to show the relative
position of the protonephridia and the coelomic
rudiment. (After Shearer.)

Letters as before, rues, larval mesoderm, consisting of ecto-
derm cells budded inwards from the second quartette.

2A

2D

2d'

FIG. 115.— Stage in the segmentation
of the egg of Nereis limbata viewed

from above, showing a laeotropic , . •, 7-1 i 1 « 1 „,"],* "

spiral cleavage of the egg. (After which Covers the post-trochal bod)

Wilson.) of the worm (Fig. 115).

;), ].oiar bodies. The third quartette is normal, but

in the case of the fourth qimrlette,

4d, termed by Wilson the second somatoblast, is formed some

considerable time before its sisters, and at once divides into right

156

INVEHTEBKATA

CHAP.

and left daughters, and these begin to found the mesodermic bands.
Wilson has recently pointed out, however (1898), that 4d is
sufficiently reminiscent of its endodermic origin to contribute six
to ten small cells to the formation of the intestinal wall.

When the larva of Nereis is fully developed, i.e. when the alimen-
tary canal has become functional, it is not only provided with a post-
trochal worm-body but this body shows the rudiments of no less than
three pairs of parapodia, and this seems to be a general feature
amongst many Polychaeta. Further, behind each pair of parapodia
is an accessory ring of cilia, so that in Nereis we have a typical
example of a Polytrochal larva. In the apical region there is to be

seen a row of five

y

gland cells — these
seem to be homologous
with the gland cells in
the upper hemisphere
of the Trochophore of
Polygordia.

The development
of the genus Cctpitclla
has been worked out
in great detail by
Eisig (1900). His
results are chiefly re-
markable for his asser-
tion that, in this form,
the mother cells of the
adult mesoderm arise
from the third and not
the fourth quartette of
rnicromeres. We are,
it seems to us, justified
in questioning this result, since it would place Capitella in opposi-
tion to every other Annelidan type which has been studied.

But Eisig records a feature from the post-trochophoral stage
which is not recorded of Polygordius, but which we have other
reasons for regarding as of an extremely primitive character, and this
is a ciliated groove stretching from mouth to anus. The same
feature recurs in Trochophore larvae belonging to quite different
groups of the animal kingdom.

ch

an

FIG. 116. — The free-swininiing larva of Nereis limbata three
days old. A typical "Polytrochal" larva. (After
Wilson.)

an, anus ; c/i, chaetae ; ell, additional ciliated rings ; r/l, gland
cells ; par, parapodia ; t.c, tentacular arms.

OLIGOCHAETA

In the Oligochaeta the prototroch is never developed at all : the
embryo develops into a blastula, which is converted into a gastrula by
invagination or by epibole. The mesoderm arises as a pole cell from
the lip of the blastopore which divides into two, and these two halves
proceed immediately to give rise to the mesodermic bands. The

VII

ANNELIDA 157

blastopore persists as the niouth, and the embryonic gut becomes
swollen and globular owing to the ingestion of the nutritive material,
the albumen," with which the embryo is surrounded.

The question of the origin of the nephridia in Annelida is a
subject which has been much worked at in Oligochaeta where, owing
to the fact that the eggs are contained in quantities in a cocoon, all
stages of the embryo up to those that show all the adult features, can
be obtained in quantity. The original conception of a nephridium
as a tube connecting the coelom with the exterior, governed the
early investigations into the subject. Bergh (1899) and Burger
(1902) asserted, that in Oligochaeta the nephridium arose as a
growth of the septal wall of the coelom, that it gave rise to a
chain of cells projecting backwards, which eventually fused with the
ectoderm and then became hollowed out, so that the whole nephridium
is to be looked on as a " tail " of the coelom. Moreover since the
first trace of a cavity appears in the funnel region and is a prolonga-
tion of the body-cavity, the cavity of the nephridium might be said
to be part of the coelom.

This view was attacked by Goodrich (1897-1898), who showed
that in certain Polychaeta (cf. Nepthys) the nephridia do not open
into the coelom at all but terminate internally in a bunch of
solenocytes which project into the coelom. He regarded the
nephridium as essentially an ectodermic structure, and as comparable
with the excretory tube of a Nemertine or of a Platyhelminth. He
believed that in a great many Annelida these blind nephridia had
secondarily acquired openings into the coelom, but that on the other
hand there were other so-called nephridia, cf. the large anterior
nephridia of Terebellidae and Arenicolidae and the nephridia of
Mollusca and Peripatus, which did actually develop as outgrowths
from the coelom, and which in consequence he termed coelomiducts.
Goodrich regards the excretory organs of Oligochaeta as " true "
nephridia not coelomiducts, i.e. as tubes originally blind which have
acquired secondary communications with the coelom, and he pointed
to the coexistence of the genital duct (which is a wide short
coelomiduct) and the nephridium in the same somite, in Lumbricus,
as evidence that the two structures cannot be homologous with one
another. Evidently the question as to which category these nephridia
belong can only be answered by renewed and exhaustive research
into the mode of their development.

This has been done by Staff (1910) in the case of the worm
Criodriliis lacuum. A word or two on Staff's method's may be in
place here. Criodrilus lacuum is a worm which inhabits swamps on
the banks of the Danube. In May and June when the swamps are
nearly dry its cocoons are found attached to the stalks of the grasses
growing in the swamp. These cocoons are collected, and they are
then pressed at one end and the contained embroyos are thus
squeezed out. They are preserved in " Eisig's mixture." Then they
are examined under a strong dissecting microscope, and slit open

158

INVEKTEBRATA

CHAP.

along the back with a fine needle. In this way the ball of albu-
minous material filling the gut can be removed, and with care the
endoderm itself can be removed. What is left consists of the meso-
dermic bands and the underlying ectoderm with its products. This
can either be cut into sections or flattened out and mounted whole.
Since development progresses from front to back, and since in one
and the same specimen well-developed coelomic cavities and nephridia
may be found in front whilst only mother cells of the mesoderm and
undifferentiated mesodermic bands are found behind, the whole
development of many organs can be elucidated by examining a few
embryos of suitable age. Staff' found that, in the case of this species,
the mother cells of the nephridia appear in the ectoderm at the

musctrc

Im.

nep.

neur

FIG. 117. — Transverse section through the ventral part of an embryo of Oriodrilus lacuiim.

(After Staff.)

me, coelomir cavity ; l.ui, first formed fibrils of the longitudinal muscles ; M.S, somite ;
niiix.cii-f, eetodermic cell group destined to give rise to the outer circular muscles ; HI/I//, eetodermic
cell group dt'st.ned to give rise to the nephridia ; new, eetodermic cell group destined to give rise to
the ventral nerve cord ; v.cil, ventral ciliated patch of ectoderm.

hinder region of the embryo, and here act as teloblasts, giving rise
to strings of cells by continuous budding off of smaller cells in front
of them, like the mesodermic teloblasts situated internally to them.
There are on each side four rows of such ectodennal teloblasts, and
the rows of cells to which they give rise become wedged in between
the ectoderm and the coelomic mesoderm. The two most ventral
rows give rise to the ventral nerve cord, the row lying immediately
outside these on each side to the nephridia, and the two uppermost
rows on each side to the external circular muscles. The last-
named teloblasts are consequently termed myoblasts.

The longitudinal muscles and the visceral muscles of Oriodrilus
and Oligochaeta generally, like those of Polygordius, are derived from
the cells of the wall of the coelom. At a later period the strings of
cells destined to give ris,e to the nephridia are broken into groups,
and one group is pushed into each septum which divides one
coelomic sac from another. Here each group grows and gives rise

VII

ANNELIDA

159

to a chain of cells, and this cell chain becomes hollowed out and
forms a tube. Its most internal cell projects into the coelomic
cavity between the coelomic cells forming one side of the septum, and
forms the greater part of the coelomic funnel of the nephridium.
The lower lip of the funnel is constituted by one huge cell belonging
to the coelomic wall. This cell (f.c, Fig. 118) only divides once and,
as is well known, the ventral lip of the nephridial funnel in the adult

coe

rtph f.c

chs

Flu. 118. — Two longitudinal sections through the ventral portion of an einliryo of
Criodrilvs lacmtm. (After Staff.)

A, section through a younger embryo in which the nephridial string is not yet broken into cell-
groups destined to give rise to the nephridia. 13, section through an older embryo in which the
nephridial string is broken into groups. Letters as before. In addition, Mtyi/i, blepliaroblasts, Le.
basal granules of cilia in the funnel of nephridium ; ch, rudiment of chaeta ; c/i.s, group of ectoderm
cells destined to form the chaeta sac ; /, funnel of uephridium ; f.v, funnel cell, i.e. tin1 large me.so-
dermic cell which, according to Staff, forms the ventral lips of the nephridial funnel ; M.T, teloblast
of mesodermic band— the two dotted lines indicate the hinder part of this band which curves outwards
so that it does not lie in the plane of the section ; nciih.st, nephridial string of cells.

worm is quite different from the dorsal lip, and consists of only two
cells. The result of this investigation is therefore to uphold Goodrich's
view.

HIRUDINEA

The development of Hirudinea is interesting for two reasons, first,
because it establishes the Annelidan affinities of this group, which

160

INVEKTEBKATA

CHAP.

we might be inclined to doubt if we were acquainted only with the
adult structure, and secondly, because it was on the embryos of
Leeches that Whitman made the first studies of " cell lineage."

We take the development of Nephelis, one of the Gnathobdellidae,

as type, because the

A kh

stom

end

mac

B

m

stom

embryology of this form
has been worked out in
recent times by Sukat-
schoff (1900, 190:3).
The egg divides as
usual into four macro-
meres and these bud off
a first quartette of
niicromeres. These
micromeres increase by
division and form the
head blastema. Of the
second quartette of
micromeres apparently
only one member is
formed, viz. 2d, the first
sornatoblast, though the
statement that cells are
budded inwards from
the first quartette of
micromeres to surround
a stomodaeum or lar-
val oesophagus looks
doubtful ; possibly re-
newed investigation
will show that these
cells are the missing
members of the second
quartette, and are
budded from the macro-
meres directly. 2d is
a large cell quite equal
in size to its sister, the
residual macromere 21).
From these two cells,
four cells of micromeric
dimensions are formed
at the vegetative pole
of the egg.

Probably we may interpret this statement thus : — from 2d, 2d2 is
budded off, which divides into 2d21 and 2d22, whilst from 21), 3d is
budded off, sole representative of the third quartette, and this divides
into 3d1 and 3d2. Whether this interpretation is justified or not, we

mac.

FIG. 119. — Two longitudinal sections of embryos of
Nephelis vidgaris. (After Sukatschoft'. )

A, optical longitudinal (frontal) section of late embryo ; B,
optical longitudinal (sagittal) section of larva just after escape
from the cocoon ; end, cells (derived chiefly from 3D) forming
definitive endoderm ; h.b, head blastema; t.b, trunk blastema;
m, mouth ; mac, degenerating macromeres ; st, stomach ; stom,
stomodaeum.

VII

ANNELIDA

161

may say at once that these " vegetative micromeres," as we may term
them, give rise to the posterior ectoderm and the external circular
muscles. They form in fact part of the trunk blastema.

The endodermal epithelium does not arise as in other Annelida
from the fourth and fifth quartettes of micromeres and from the
equal division of the residual macromeres, but by the budding of a
single cell from the residual macromere 2B, and of several cells from
the residual macromere 4D. The residual macromeres in the
quadrants A, B, and C, after having undergone the divisions recorded
above, give rise to no more cells ; they become smaller and smaller as
development goes on, and are finally absorbed. The cells destined to
form the lining of the alimentary canal lie between them, and the
remains of the macromeres

are thus found outside the mac

alimentary canal ; a contrast
to the condition of affairs
obtaining in the Ehynco-
bdellidae as represented by
Clepsine, where the endoder-
mal cells are budded from
the surfaces of all four macro-
meres and surround them.

Thus, in one group of
leeches the endoderm is
formed from practically only
one macromere, and lies in-

side Surrounded by the four FlG. 120.— A fairly advanced embryo of Clepsine
macromeres, whilst ill another

group of leeches, the Ehyn-

including

&

(Glossiphonia)

Whitman.)

seen from behind. (After

forming definitive endoderm on the outer

/'/"v; '7 1 surface of mac, degenerating macromeres; ltd, trunk

(MOSSlpnOma) and blastema of right side; tlft, trunk blastema of left side.

its allies (Fig. 120), the
endoderm is formed from all four macromeres and lies outside
them. "We conclude that both forms of development are modifica-
tions of a primitive type, such as is seen in Polygordius and most
Polychaeta, in which the residual macromeres are directly converted
into the endodermal epithelium ; and we are reminded of somewhat
similar differences in endoderm formation between Siphonophora and
other Hydrozoa, amongst Coelenterata (Chap. IV), and between
Planocera and Yungia amongst Platyhelminths (Chap. V).

In Nephelis, after the endoderm is formed, a transverse row <>!'
ten cells can be discerned at the hinder end of the embryo. Of these,
two are situated more internally than the rest, and these two are the
teloblasts of the true coelomic mesoderm and owe their origin to the
division of 4d, the sole member of the fourth quartette to be formed.
The remaining eight owe their origin to the division of the four
" vegetative micromeres " mentioned above. Of the eight, the two
nearest the mid-ventral line are termed neuroblasts, because they

VOL. i M

162

INVERTEBEATA

CHAP.

give rise by budding to strings of cells which will form the ventral
nerve-cord. Outside these are two cells termed " nephridioblasts,"
which give rise to strings of cells which separate into groups as the
body of the embryo leech lengthens, and form the nephridia. Outside

these again are the myoblasts, which
similarly give rise to cells which form
the external circular muscles, whilst
finally the two most external cells
give rise to strings of cells which
broaden out and form the posterior
ectoderm. All these strings of cells
taken collectively constitute the trunk
blastema, it will be thus seen that the
development of the trunk blastema is
almost identical in character in Crio-
drilus and Neplielis.

A few of the nephridia which are
formed at first grow to relatively
enormous dimensions, and function as
excretory organs during development
(Sukatschoff, 1900). "These larval
nephridia later disappear, and one is

involuntarily reminded of the fate which befalls pronephros of
Vertebrata (Figs. 121 and 122).

At first the head blastema is widely separated from this trunk
blastema by a large expanse of bare macromeres : in a typical
annelidan embryo this expanse would be taken up by the prototrochal

mac

FIG. 121. — Hinder view of a well de-
veloped larva of Neplielis
(After Sukatschoff. )

Letters as before. In addition,
larval nephrida.

ie

Ineph

l.neph2

FIG. 122. — Larva of Nephelis viilyaris viewed from the side. (After Sukatschofl'.)

l.Hi'iihl, the anterior, and?. nephP, the posterior larval nephridhim ; e.o, external opening of one side
of nephridiuin ; i.e, internal blind end of nephridiuin ; A, anterior end of larva ; D, dorsal surface of
larva ; P, posterior end of larva ; [', Ventral surface of larva.

cells, which are absent here in accordance with the absence of a free
larval stage. The strings of cells forming the ectoderm of the trunk
blastema rapidly grow forward, beneath them are the two deeper
strings formed by the budding of 4ar and 4d', the mother cells of the
mesoderm which have arisen by the division of 4d. The trunk

vii ANNELIDA 163

blastema at first meets the head blastema ventrally, then it
subsequently extends up at the sides of the embryo and envelops the
dorsal region.

Long before this the mesodermic bands have developed within
them a double series of coelomic cavities. These rapidly meet one
another above the nerve-cord and form the ventral sinus, they then
extend upwards at the sides of the alimentary canal and meet above
it forming the dorsal sinus. The septa, which at first would
naturally separate each coelomic sac from those anterior and posterior
to it on the same side, disappear in the region of the dorsal and
ventral sinuses, but laterally they thicken and form the great mass
of connective tissue which makes up the " parenchyma " of the leech,
and the cavities of the coelom between them are thus reduced to
narrow slits.

We may note that in Clepsine (Glossiphonia) the dorsal angles of
the coelomic sacs, as they extend upwards towards the mid-dorsal line,
bear a row of cells called "cardioblasts." These cells when they
meet their partners (viz. when the right one meets the corresponding
left one) form the wall of the dorsal blood-vessel ; the lumen of the
vessel arises from the fusion of a string of vacuoles formed in the
cells. This dorsal blood-vessel is absent in the Gnathobdellidae.

ALLIED FORMS

Iii old classifications of Annelida a group termed Gephyrea
appears. This group is now totally broken up into three distinct
phyla, of the Echiuroidea, Priapuloidea, and Sipunculoidea. Of these
the last named possess a Trochophore larva and a most interesting
development, which will be dealt with later on, but which is most
assuredly not Annelidan in character. The development of the
Priapuloidea is entirely unknown.

The Echiuroidea, however, possess a development which proves
them to be modified Polychaeta. The embryo starts free-swimining
life at a post-trochophoral stage comparable to that in which Nereis and
its allies begin their larval life. There is a well-marked trochophoral
"head," followed by a worm body with numerous closely adpressed
somites, which, however, do not develop parapodia. There are well-
developed protonephridia, and an apical plate and prototroch, a
ventral ciliated groove and larval muscles. The segments disappear
in the adult, which exhibits a simple undivided coelom, and a nerve-
cord with no ganglionic thickenings.

AFFINITIES OF ANNELIDS

We have now completed our survey of the various types of
Annelid development, and it will be seen that they are all easily to
be interpreted as abbreviations and simplifications of the long larval
history characteristic of Polygordius. The primitive nature of

164 INVEKTEBRATA CHAP

Polygordius, which is deducible from the anatomy of the adult, is fully
borne out by a study of its development.

When we turn to the development of the Annelida for light as to
the origin of the phylum, the question to be solved resolves itself
into the question of how the Trochophore larva is to be interpreted.
We have already anticipated the answer to this question in dealing
with the Pilidium larva of Nemertinea ; we interpreted that larva as
representing, in a simplified form, an ancestor which, if it were living
now, would l)e classed as a Ctenophore.

But the Trochophore of Polygordius, at the stage when mouth and
anus are still not separated, presents an even closer resemblance to a
primitive type of Ctenophore than does the Pilidium larva. For the
four discrete groups of ciliated cells which have not as yet united to
form the prototroch, may be regarded as representing shortened
ciliated ribs. Further, Woltereck has shown that beneath the ciliated-
apical plate are ganglion cells and fibres, and that from this centre,
radial nerve strands extend out to the groups of ciliated cells which are
supposed to represent the ribs, just as nerve strands radiate from the
polar plate underlying the ribs in Ctenophora.

The likeness of the larval muscles to the contractile strands of
Ctenophora has already been chvelt on in the case of the Pilidium,
and need not be further insisted on here, but the fact that four, not
eight ribs are developed in the Trochophore need not disturb us,
especially in view of the fact (see p. 92) that the eight ribs of the
Ctenophore are represented in the embryo by four radiating streaks
of small cells, and that it is therefore independently probable that in
some ancestral Ctenophore there would be four, not eight ribs.

We should thus have three distinct larval types, viz. Muller's
larva, the Pilidium, and the Trochophore, all representing, with more
or less modification, a group of ancestral Ctenophora from which
sprang the Polyclada (and through them all Platyhelminthes), the
Nemertinea and the Annelida.

The Polyclada are essentially ground Ctenophora which glide over
the substratum instead of swimming freely through the water, and
Ctenoplana seems to be a modern Ctenophore beginning to undergo
a change similar to that undergone by ancestral Ctenophores when
they became Polyclada.

As to the nature of the changes which the ancestral Ctenophore
underwent in becoming a Neinertinean, \ve shall not hazard an
opinion until the metamorphosis of those worms has been more
thoroughly analyzed.

Woltereck, however, attempts to sketch the course of the changes
which the Trochophore underwent in becoming an Annelid. He
supposes that as it grew older the animal developed the habit of
dropping to the bottom and taking to a burrowing habit, whilst still
retaining its free-swimming habits during its youth. As a conse-
quence the trochophoral ciliated cells were rubbed off, and the gap in
the ectoderm thus caused was closed before and behind by prolifera-

vii ANNELIDA 165

tions of cells from the intact ectoderm. In this way he accounts for
that characteristic feature of development, the casting off of the
prototroch and the union of the head and trunk blastema. The
segmentation of the niesoderm and coelom he brings into connection
with the wriggling method of progression which replaced ciliary gliding.

It is worthy of note that on this hypothesis, segmentation can only
have appeared after the burrowing life was assumed, and the appear-
ance of segments in the free-swimming larva, which is seen even in
Polygordius, must be regarded as a " telescoping " of development in
comparison with what actually occurred in the history of the race.
To similar conclusions we are driven by the study of almost all
classes of larvae, so there is nothing unlikely in Woltereck's theory,
which we may indeed provisionally adopt as by far the best solution
of the problem of the origin of the Annelida which has as yet been
offered.

We have, however, another problem to face. There appears in
the Annelida for the first time, an organ widely distributed in the
animal kingdom, over whose nature and origin many battles have
been fought. We refer to the coelom, often aptly termed by the
German authors the secondary body-cavity in order to distinguish
it from the space which first appears in the embryo termed the
segmentation cavity or blastocoele ; the segmentation cavity is
termed by the Germans the primary body-cavity, and it forms
the space intervening between skin and gut in the Trochophore.

Now the investigations of the American authors show, that the cells
forming the wall of the coelom always originate by the division of a
single cell 4d, whose sisters 4a, 4b, and 4c, enter into the formation
of the endodermic wall of the gut, while 4d itself contributes cells to
the gut wall. It is, therefore, reasonable to suppose that 4d itself at
one time formed part of the endoderm, and that the adult mesoderm
is of endodermic origin. The final demonstration of this belongs to
Shearer (1911), who has shown that in Eupomatus 4d actually forms
part of the endodermic wall of the larva for a whole day after the
free-swimming life has begun.

T>ut what changes in successive generations of adults can we
suppose to be represented by the separation of a gut -cell from its
neighbours, and by its proliferation to form a mass of cells which
later become hollowed out to form a cavity ? By far the easiest and
most natural suggestion is that the process in the larva represents
the separation of a pair of endodermal pouches or of a single bilobrd
pouch from the gut, which eventually became completely shut off
from the main gut and devoted to other uses. This interpretation is
borne out in the strongest manner by the actual origin of the coelom
in other groups where it occurs, and when we are treating of the
Echinodermata the question will be discussed more fully.

The alternative theory which was originally put forward by
Meyer (1887) is, that the separation of the mesodermic cells from the
gut wall represents an outward migration of the primitive genital

166 INVEETEBEATA CHAP.

cells, and that in the ancestral form the genital cells formed compact
packets lying at the sides of the gut, and at maturity burrowed their
way out as they do in Nemertinea. In later stages of the race it
is supposed that after the main mass of cells were dehisced, a peri-
pheral layer was retained and formed the wall of a hollow sac, thus
constituting the primitive coelomic sac, which on this supposition
was a " gonocoele." It is further supposed that in course of time
what were originally genital cells became modified into longitudinal
muscles and excretory yellow cells, both of which in Annelida are
formed from the coelomic lining.

Now this latter theory seems to fit in well with certain facts. It
serves to connect the Annelida and the Nemertinea, and it is
undoubtedly true that at the period of sexual maturity in Poli/gordius
and in many Polychaeta the coelomic cavities become absolutely blocked
up by the mass of genital cells which have been proliferated from their
walls. But it is a little disconcerting to find that, whereas, according to
theory, the coelomic cavity should not appear till after the main mass of
the genital cells has been dehisced, and that the surviving cells should
then be converted into peritoneum and peritoneal muscles, in actual
development, as a matter of fact the cavity appears first and the
peritoneal muscles are differentiated a long time before there is any
trace of genital cells. Further, when these genital cells finally do make
their appearance and are dehisced, far from the worm taking on a new
lease of life, which, according to the theory, must have constantly
occurred in some ancestral stock, the animal dies and all its tissues
disintegrate. Why the ancestral animal should wait to form muscles
till the main purpose of its life has been fulfilled, and what it used for
muscles in the meantime, are questions very difficult to answer on
this theory.

The theory, however, as we have already said breaks down when
other groups of the animal kingdom are studied, unless we are
prepared to assume that a fundamental organ with essentially
constant character like the coelom, originated from totally different
rudiments in different groups, a view which would be subversive of
all the recognized principles of reasoning in comparative anatomy.
When finally we consider, as all zoologists allow, that the Annelida
are derived from Coelenterata, and when we observe that in Scyphozoa,
Actinozoa, and Ctenophora, the primitive gut tends to lie divided
into a central digestive portion and peripheral branches whose walls
give rise to muscle cells, and in some of which the genital cells
ultimately appear, it seems to us that there can be but one opinion
as to which theory of the coelom is the more inherently probable ;
indeed it is only in consequence of the myopic concentration of
attention on the facts of development in a limited number of groups,
and the neglect of the facts of development in other groups, that
the gonocoele theory ever has obtained any vogue.

The most characteristic feature of Annelida, next to the segmented
coelom, is the nervous system, consisting of brain, collar, and ganglion-

vii ANNELIDA 167

ated ventral nerve-cord. The brain is, of course, to be compared to
the ganglion cells underlying the apical sense-organ in Ctenophora,
which have been experimentally proved to act as a co-ordinating
centre for the ciliary activity of the ribs. The ventral nerve-cord
originates as two longitudinal thickenings of the ectoderm, situated
at the sides of the mid-ventral line.

Now in many larvae in the post-trochophoral stage (of. Echiuriis,
Oapitella), the mid- ventral line is occupied by a ciliated groove. This
groove extends from the metatroch behind the mouth to the telotroch
just in front of the anus, and thus it corresponds roughly to the
portion of the blastopore which closes in the process of separation
of primitive mouth from primitive anus. This process in the history
of the race must have been an extremely gradual one, and while the
undivided opening was in the figure-of-eight stage the whole circuit
of its lip was probably fringed with cilia, whose activity would assist
in the seizing of food. Just, then, as there is a ring-nerve underlying
the prototroch, so we might expect to find nerve fibres underlying
this ciliated border, and out of these nervous strands we may suppose
the ventral nerve-cord to have been built up. If such a circurn-oral
nerve existed in the original creeping Ctenophore it would certainly
l)e connected with the nerves radiating from the apical centre, and
one pair of these connections may have persisted as the nerve collar.

The nephridia — here essentially similar to those of Nemertinea
and Platybelminthes — are a new acquisition. The original function
of getting rid of excreta would be naturally concentrated in the
ectoderm. When, owing to increase in size and muscular activity,
the excretory surface of the ectoderm became insufficient for this
purpose, ingrowths and in foldings would take place which would
increase its surface and its efficiency, and these ingrowths we suppose
to have given rise to the primitive nephridia ; and their embryonic
history bears out this view.

It would be an extremely interesting thing to investigate the
excretory processes in Ctenophora, for thus it is possible that the first
fore-shadowings of primitive nephridia might be discovered. But by
no means all the excretory work in a Coelenterate is performed by the
ectoderm, since the endodermal cells also get rid of some excreta into
the gut cavity, whence it is ejected to the exterior. This function would
still be carried on by the lateral pockets of the gut, when they were
separated from the main axial portion as coelom. Thus the coelomic
lluid would tend to become charged with excreta, and so it would
have to be periodically got rid of. This would be facilitated by the
formation of coelomic pores, such as actually occur in the earthworm,
and it seems to have also been accomplished by the fusion of the
coelomic wall with the tubes of the ectodermal nephridia, a process
which Groodrich believes to have given rise in some cases to the
internal funnels of these nephridia, when they occur. In many cases
also the genital duct, which originated as a coelomic pore, is utilized
for this purpose, and in this way the larger trumpet -shaped

168 INVERTEBRATA CHAP, vn

nephridia of certain groups, such as the Arenicolidae, may have
been formed.

According to the view thus outlined the Annelida would be
another instance of a degenerate bottom-living off-shoot from a
primitive pelagic group of animals.

LITERATURE REFERRED TO

Bergh. Nochmals iiber die Eutwickelung der Seginentalorgane. Zeit. fur \viss. Zoo!.,
vol. 66, 1899.

Burger. Weitere Beitrage zur Entwickelungsgeschichte der Hinulineen : Zur
Embryologie von Clepsine. Zeit. fiir wiss. Zool., vol. 72, 1902.

Child. The Early Development of Arenicola and Sternaspis. Arch. Ent. Mech.,
vol. 4, 1900.

Eisig. Zur Entwickelungsgeschichte der Capitelliden. Mitt. Zool. Stat. Neap.,
vol. 13, 1900.

Fraipont. Le genre Polygordius. Fauna und Flora des Golfes von Neapel, 14,
1887.

Goodrich. On the Nephridia of Polychaeta. Part I. Quart. Journ. Mic. Sci., vol.
40, 1897. Part II. Ibid. vol. 41, 1898.

Meyer, E. Die Korperbau der Anneliden. Mitt, ans dem Zool. Stat. Neapel, vols. 7
and 8, 1887.

Shearer. On the Development and Structure of the Trochophore of Hyilroidfs
vnciniitus (Eupomatus}. Quart. Journ. Mic. Sci., vol. 13, 1911.

Staff. Organogenetische Untersuchungen iiber Criodrilus Jacuum. Arb. aus dem
Zool. lust. Wien, vol. 18, 1910.

Sukatschoff. Beitrage zur Entwickelungsgeschichte der Hirudineen. I. Zur
Kenntniss der Urnieren von Ncphelis vulgaris und Aulustomus galo. Zeit. fiir wiss.
Zool., vol. 67, 1900.

Sukatschoff. Beitrage zur Entwickelungsgeschichte des Hirudineen. II. Uber
F urduing und Bildung der embryonalen Anlagen bei Nephelis vulgaris. Zeit. fiir wiss.
Zool., vol. 73, 1903.

Tredwell. The Cytogeny of Podarke obscura. Journ. Morph., vol. 17, 1901.

Whitman. The Embryology of Clepsinc. Quart. Journ. Micr. Sci., vol. 18, 1878.

Wilson, E. B. The Cell-Lineage of Nereis. Journ. Morph., vol. 6, 1892.

Wilson, E. B. Considerations on Cell-Lineage and Ancestral Reminiscences. Ann.
New York Acad. Sci., vol. 11, 1898.

Woltereck. Beitrag zur praktischen Analyse der PoZj/gwdms-Entwicklung nach
dem Nordsee- und dem Mittelmeertypus. (1) Der fiir beide Typen gleichverlaufende
Entwicklungsabsclmitt vom Ei bis zum jiingsten Trochophora stadium. Arch. Ent.
Mech., vol. 18, 1903.

Woltereck. Trochophorastudien. I. Uber die Entwiekelung des Annelides bei den
Poly {ford iusiwim der Nordsee. Zoologica, 1902.

Woltereck, Zur Kopflrage der Annelideu, Verh. Deutschen Zool. Ges., 1905.

CHAPTER VIII
AKTHKOPODA

Classification adopted—

Trilobita. Pantopoda.

Prototracheata (Onychophora). Myriapoda.

Crustacea. Insecta.

Arachnida. Tardigrada.

THE great group of the Arthropoda comprizes at least two-thirds of
the species of animals now existing, besides a large proportion of
those extinct forms whose remains are preserved as fossils. Of the
existing species belonging to the group the greater number are
included in the enormous classes of Crustacea, Arachnida, and Insecta.
The Myriapoda is a class which can only be described as a lumber-
room, since it contains some species which have close affinities
with the Insecta and others of widely different relationship. The
Prototracheata, Pantopoda, and Tardigrada are small classes including
comparatively few species. The Trilobita is a large class, but all the
species comprizing it are now extinct and are known only from their
fossil remains.

It is generally conceded by zoologists that an Arthropod is
merely a further development of the annelidan typo of structure.
The two groups Arthropoda and Annelida agree in having their
bodies built up by a metameric repetition of similar segments, and in
the structure of the central nervous system. The most primitive of
living Arthropoda are the Prototracheata or Onychophora ; they
possess a series of so-called nephridia metarnerically arranged which
correspond to the coelomiducts of Annelida, and they are on this
account excluded from the Arthropoda altogether and reckoned as
Annelida by some naturalists.

The true relationship which Prototracheata, and through them
the rest of the Arthropoda, sustain to the Annelida was made clear
by the classic researches of Sedgwick on the development of
Peripatus capensis (1885-1888). We cannot select this or any other
species of Peripatus as a type for special description because of the
extreme rarity of the animals belonging to this genus, but it is

169

170

INVERTEBRATA

CHAP.

necessary to give a brief account of the principal points elucidated
by Professor Sedgwick, in order that we may have a correct appre-
hension of the significance of the development of other Arthropoda.

PROTOTRACHEATA (ONYCHOPHCRA)

The embryo of Peripatus capensis passes through its entire
development within the oviduct of the mother, and it is born in a
form in which it already exhibits all the essential features of the
adult. The egg is very minute and, like the eggs of many Insecta,
is of an elongated ellipsoidal shape, its longest axis measuring about
•4 mm. It is telolecithal, that is to say that there is a darker area
with a minimum of yolk and a maximum of cytoplasm situated at
one end of the shortest axis of the ellipsoid, whereas the rest of the
egg is paler in colour and richer in yolk. Segmentation is complete ;
the first four segments formed by the first two cleavages are of the
same size, but the third cleavage separates off four smaller darker
" animal " cells from four larger paler " vegetative " cells. The first-
named by rapid division
give rise to the ectoderm,
the latter to the endo-
derm.

AVhen segmentation
is completed, the endo-
derm consists of a num-
ber of larger cells loosely
connected one with
another by strings of
cytoplasm which occupy
most of the space within
the egg membrane, the
ectoderm on the other
hand forms a cap of
small closely aggregated
cells which are also
connected together by
filaments of cytoplasm
(Fig. 12:5 A).

Sedgwick justly at-
tached considerable im-

have begun to grow over them (epi bole). C, the covpring-in of pOltailCe to tllCSe C011-

necting filaments, and
held that they upset
the popular conception
of a cell as an isolated unit, and of a Metazooii animal as a
mere collocation of such units, or as a colonial Protozoon. He was
inclined to regard a multinucleate Protozoon, such as Actinosphaerium,
as t<;ivinu- a better idea of the common ancestor of Metazoa. Most

o o

end

Fin. 123. — Stages in the segmentation and the gastrula-
tion of the egg of Peripatus tw_/»v/.s/\. (After
Sedgwick.)

A, conclusion of segmentation. The ectodermic cells form a
small cap resting on the endoderm cells which are loosely dis-
persed within the egg membrane. B, the endodermic cells are
contracted so as to form a compact mass, and the ectodermic cells

the endoderm cells is almost complete — a few endoderm cells
protrude through the blastopore. irt, ectodermal blastomeres ;
einl, endodermal blastomeres.

viii AKTHROPODA 171

colonial Protozoa are found, however, when closely examined, to
exhibit similar strings of cytoplasm connecting together the various
individuals which make up the colony, and so the opposition between
the two views tends to disappear.

The mass of scattered eudoderui cells undergoes contraction, its
units being drawn closely together, so that it forms a compact group
of cells, and then the ectoderm grows over its sides and completely
invests it, leaving only a small area in the centre of the vegetative
pole uncovered. At this spot the large rounded endoderm spheres
protrude for a time (Fig. 123 C). Soon a cavity is formed in the
centre of the endodermic mass, by the formation of vacuoles which
coalesce with one another. This cavity, which is the archenteron,
opens to the exterior by an aperture, the blastopore, in the centre
of the uncovered area of endoderm, and so the process of gastrulation
is completed.

The gastrula, which had become nearly spherical, now again
elongates, and the blastopore becomes elongated also. Behind it there
appears a darker area which seems to be an area of rapid proliferation
in the endoderm, this is named by Sedgwick the primitive streak.
From this area there is produced a crescentic mass of cells lying
beneath the endoderm, the two horns of which grow forwards at the
sides of the blastopore and constitute the two mesodermic bands.

In the meantime the elongated blastopore becomes divided by a
constriction into two apertures, the anterior of which persists as the
mouth whilst the posterior remains as the anus. The mesodermic
bauds then became divided into blocks termed somites, in each of
which a cavity, the coelomic cavity, appears (Fig. 124).

For some time the blastopore is considerably less in length than
the embryo, so that there is a prae-oral as well as a post-anal gut, or
to put it in another way, there is a short ventral surface and a very
long arched dorsal one. The prae-oral and post-anal gut finally
disappear owing to the greater relative growth of the ventral surface.

The reader will not fail to observe that up to this stage there
is a remarkable general resemblance between the development of
Peripatus and that of an annelid. The formation of a cap of small
ectoderm cells resting on larger endoderm cells and gradually
investing the latter by the process termed epibole ; the division of
the blastopore into mouth and anus; the formation of mesodermic
bands from endoderm cells in the posterior lip of the blastopore, and
their division into metamerically arranged somites, in each of which
a cavity appears; — all these are features which have become famili;ir
to us in our study of the development of Annelida.

But from this stage onwards distinctively arthropodan features
make their appearance. The rudiments of appendages appear as pairs
of protrusions of the ventral ectoderm arranged metamerically behind
one another in correspondence with the somites; the first to <ippr;ir
are the antennae which are at first situated at the sides of the mouth,
but which later, along with the corresponding somites, shift forwards

172

INVEKTEBKATA

CHAP. VIII

to a prae-oral position ; the other appendages develop in order from
before backwards. Into each rudimentary appendage an outgrowth
of the corresponding somite with its coelomic cavity extends. Then
the endodermic tube shrinks away from the ectoderm and leaves

m

som

-ps

Vm. T24. — Stages in the division of the blastopore and the formation of the inesoderm of

I'crijmtits capcnsix. (After Sedg"\vick.)

A, the blastopore elongated but unconstrictt'd ; the primitive streak is seen behind the blastopore..
B, the blastopore has .just divided into mouth in front and anus behind. The mesodermic bands
have been formed and have already budded off somites in front. C, the embryo has become concave
ventrally. The appendages are beginning to grow out from the somites, a, anus ; ap, appendage ;
nt, rudiment of antenna ; '</./<, blastopore; m, mouth; y.s, primitive streak ; mini, somites.

spaces which eventually form the body-cavity of the adult, a cavity
which is totally distinct from the coelom and is termed the haemo-
coele since it becomes tilled with blood (Gr. liaciiut, blood). It corre-
sponds exactly to the blastocoele or primary body -cavity of the
Annelid larva. Of these spaces three primary ones may be dis-
tinguished, namely, one median ventral and two dorso-lateral (Fig.

174 INVERTEBRATA

CHAP.

125 A). By the further shrinkage of the endoderm the two dorso-
lateral spaces fuse into one median dorsal space which subsequently
forms the cavity of the heart. Inasmuch as this space is wedged in
between the dorsal apices of a pair of somites, it corresponds both in
origin and position to the dorsal blood-vessel of Annelida.

Meanwhile each somite has become divided into a dorsal portion
lying at the side of the median blood-space, and a ventral portion lying
in the base of the corresponding appendage. The walls of both
portions, but especially of the latter, give rise by proliferation to a
great mass of cells which fills up the appendage and clings to the
side of the gut. In this mass other blood-spaces make their
appearance. First appears a space in each appendage which
embraces the tip of the ventral division of the coelom and forms the
cavity of the leg in the adult. This we may term the appendicular
sinus. Then comes a space nearer the inid ventral line, above the
spot where the nerve-cord is formed. The nervous sytem arises in the
typical annelidan manner as two ventral band-like thickenings of
the ectoderm which remain widely separated in the middle line, but
which meet one another in front of the mouth and behind the anus.
The brain arises as two thickenings of the prae-oral lobe where these
bands meet in front.

The blood-space above each half of the nervous system forms the
lateral sinus of the body cavity of the adult, and it remains separated
from the appendicular sinus and also from the median ventral blood-
space by a strand of cells. Above it, at the sides of the gut and
external to the dorsal divisions of the coelom, two other spaces appear
at each side.

The dorsal division of the coelom, in most of the segments of the
body, collapses and forms a flat plate of cells from which the side of
the heart and one half of the pericardial septum are formed. One
pair of the spaces which lay externally to these parts of the coelom,
meet above the plates of cells which result from the collapse of the
coelomic cavities and form the pericardium ; the other pair meet
above the gut and form the dorsal division of the general body-cavity.
This dorsal division of the haemocoele coalesces with the median
ventral space and forms the general perivisceral cavity of the
adult. The ventral division of the cavity of the somite (somz, Figs.
125 C and D) — i.e. the true coelom — persists as a thin- walled vesicle
from which a coiled tube, the excretory organ, the so-called
" nephridium," grows out and, fusing with the ectoderm on the inner
side of the leg, forms there a pore which is the external opening of
the nephridium. Finally the nervous system separates from the ecto-
derm, forming two parallel nerve-cords, and between them and the
ectoderm, of which they originally formed a part, a sub-neural sinus
is formed.

The ectodermic thickenings from which the nerve -cords have
broken away, remain for a long time visible, and are termed by
Sedgwick ventral organs. They gradually approach each other in

V11I

AETHEOPODA

175

the mid- ventral line, and it has been surmized that they are a last
reminiscence of the ventral ciliated groove which extends between
mouth and anus in many Annelid larvae.

In certain of the hinder segments of the body the dorsal divisions
of the coelom, after giving rise to the lateral walls of the heart and
to the pericardial septum, do not utterly collapse, but retain narrow
cavities. The somites belonging to several successive metameres
fuse with one another so as to form two longitudinal tubes which
constitute the genital organs (Fig. 125 D). In the penultimate
segment the division of the somite into dorsal and ventral portions does
not take place ; the excretory organ which belongs to this segment
forms the lower portion of the genital duct, whilst the upper portion
of the same duct is formed by the undivided coelom belonging to
that segment.

FIG. 126. — The formation of the appendages in the embryo of Peripatus ci<i><'iu<ix.

(After Sfdgwk'k. )

A, side view of an embryo in which the appendages are in process of formation, to show tlie \enii-al
concavity and the dorsal hump. B, ventral view of the head of a much older embryo, fn shou \\\<-
cerebral groove and the lip which surrounds the Imccal cavity, at, antenna ; c.g, cerebral groove ; gn,
gnathite (jaw) ; ijn.b, swelling at base of jaw ; /, lip enclosing buccal cavity ; or.]), oral papilla.

It remains to be added that a stomodaeum and proctodaeum
are formed by ingrowths of ectoderm round the lips of the original
mouth and anus, which displace these openings inwards; that on
the under side of the ectodermal thickenings, which give rise to the
brain, two deep pits are formed termed the cerebral grooves (<•.//,
Fig. 126 B) which later become closed off from the exterior, and form
for a time hollow appendages of the brain ; that the outer buccal
cavity which envelops the jaws is formed by the growth of a semi-
circular fold (7, Fig. 126 B) ; that the salivary glands are the excre-
tory organs belonging to the jaw segment, from the tubes of which
glandular pouches grow out, which project backwards ; and finally,

176 INVERTEBRATA CHAP.

that the slime glands, which open on the oral papillae and secrete
the silk with which Peripatus spins its web, are of ectodermal origin,
as are also the crural glands which open on the inner side of the
legs external to the openings of the excretory tubes. The tracheae
develop from simple ectodermal ingrowths which arise very late in
development. The eyes are simple and formed like the eyes of Mollusca,
'as vesicles which become closed off from the exterior. A cuticular lens
is secreted by the cells of the anterior wall, and the cells forming the
posterior wall become the visual cells. The whole organ resembles the
"ocellus "of an Insect larva and the cuticular lens inny.be compared
to the "glass body" of the latter (see Fig. 219).

From this necessarily brief and condensed sketch of Sedgwick's
results, it will be seen that the change from the annelid to the
arthropod type of structure must have been accompanied by a
suppression of the coelom and an enlargement of the blood-spaces,
the latter forming the functional perivisceral cavity of the adult,
while remnants of the former persist in the end-sacs of the excretory
organs and the cavities of the generative organs.

This change was also accompanied by an intensification of the
secretion of cuticle, and it is just conceivable that this intensifica-
tion of the secretory powers of the ectoderm entailed the other
changes which supervened. If chitin be allied to uric acid, as has
been asserted, and if the production and casting off of chitin can be
likened to nitrogenous excretion, then we may understand how the
coelomic wall, which had previously undertaken a considerable portion
of this function, might become relatively unimportant and might
tend to dwindle and disappear.

In Peripatus the chitinous cuticle is thinner and more flexible
than in any other known Arthropod, and in no other Arthropod is
a continuous series of " uephridia " retained. In all others the cuticle
is thicker and the " nephridia " are reduced to one or a very few pairs ;
in some cases they seem to be absent altogether. Cuticle and
" nephridia " seem therefore to vary in development inversely to one
another, and since increase in cuticle seems to entail decrease in
" nephridia," it may well be that the same factor has led to the
decrease and disappearance of the coelom.

VIII

AETHROPODA

177

CEUSTACEA
Classification adopted —

' new terms invented bij Caiman (1909) have not been universally
They are yivcn in

I. Phyllopoda

Branchiopoda

I Cladocera
II. Cirripedia

III. Ostracoda

IV. Copepoda

V. Malacostraca
Leptostraca
Anaspida
Stomatopoda .

flsopoda
Arthrostraca Anisopoda

[AmpMpoda
Cumacea

I Mysidacea

I Euphausidacea

Schizopoda

(Phyllocarida)

(Syncarida)

(Hoplocarida)

(Peracarida)

Decapoda

Macrura

Anoraura
Brachyura

[Penaeidea
| Caridea

Nephropsidea

Loricata

(Eucarida)

When we now turn to survey what is known of the development
of other Arthropoda we find that Insects and Arachuida exhibit,
clearly and obviously, a comparatively slight modification of the type
of development exemplified by Peripatus. But Crustacea have a
development which is not so obviously referable to this type. One
or two Crustacea are said to have total segmentation of the egg. The
best known case of this is the Penaeid shrimp Lucifer as described
by Brooks (1882). With these exceptions the eggs of all Crustacea,
Myriapoda, Insecta, and Arachnida have incomplete segmenta-
tion, and all, including those which have total segmentation, have
the peculiar disposition of yolk known as centrolecithal.

The eggs of Peripatus capensis and of allied species are the only
Arthropodan eggs which could properly be described as telolecithal.
In a centrolecithal egg the yolk is densest in the interior of the egg,
and it is surrounded by a skin or rind of cytoplasm. Often the
nucleus of the ripe egg is situated near the centre in a sort of island
of cytoplasm, but when it divides the daughter nuclei wander
outwards and take up their places on the exterior ; consequently a
segmentation of the egg results which is apparently total but is in
reality superficial, for the cleavage planes dividing the blastomeres
from one another extend only a limited distance inwards, so that

VOL. I N

178 INVEETEBEATA CHAP

internally all the blastomeres merge in an uusegmented mass of yolk.
If this superficial segmentation occurs only on one side of the egg—
i.e. if the daughter nuclei migrate only to one part of the surface—
the segmentation becomes meroblastic, although, as we shall see,
this meroblastic segmentation differs most markedly from that found
in Cephalopoda, which is derived from the telolecithal method of
development.

ASTACUS FLUVIATILIS

We select as type of Crustacean development that of the common
river crayfish Astacus fluviatilis. A full description of the develop-
ment of this form is given by Eeichenbach (1888), and no such
thorough account of the development of any other form has been
given before or since.

As every one knows, the eggs are carried throughout their entire
development by the mother, attached to her swimmerets by a glutinous
secretion. Eeichenbach found that when the eggs were removed
from the parent they quickly degenerated and died. In the case of
the allied genus the Lobster (Homarus), it is perfectly feasible to rear
the eggs after they have been removed from the swimmerets of the
mother, but in order to do this an elaborate arrangement must be
provided so as to secure a constant supply of fresh aerated water to
bathe the eggs and to ensure that they shall be constantly agitated.
Such an apparatus is provided in the various lobster hatcheries
built and maintained by the Canadian and United States govern-
ments. In default of such apparatus the plan adopted by Eeichenbach
seems to be efficient and simple, viz. to keep a large number of
females carrying eggs in an aquarium, and from time to time to
remove a portion of their brood for examination.

By means of very simple arrangements the females can be kept
for a long time in a state of perfect health. If the bottom of the
tank be covered with only a few inches of water, and provided with
an overflow ; if a slender stream be kept constantly falling into the
tank from a tap ; if the tank be provided with a covering of wire-
netting in order to prevent the crayfish escaping ; and if the whole
tank be kept shielded from direct sunlight— then all the conditions
will be fulfilled necessary to maintain the crayfish in a healthy
condition. They are easily fed on earth-worms, scraps of fish, etc.

All the eggs belonging to any one female are in the same stage of
development at one time, but the period required "for complete
development is a very long one, extending over several months.
Thus, by keeping together a large number of females with eggs in
very different stages of development, a complete series of stages can
be picked out in a very much shorter time than would be required
if the eggs of the same female were taken for all stages.

The eggs of the crayfish, like those of most Arthropoda, are very
difficult to deal with, as they are composed chiefly of semifluid yolk
enclosed in a very tough resistent membrane, and if an attempt be

VIII

AETHKOPODA

179

made to remove this membrane, the fluid mass flows out and the
egg is destroyed; so Keichenbach recommends the following pro-
cedure. The eggs are carefully removed from the parent and are
placed in water which is slowly heated to 70° C. ; then they are further
hardened by being immersed in a 2 per cent solution of bichromate
of potash for twenty-four hours ; then they are soaked for twenty-
four hours in distilled water, which is often changed ; and finally,
they are transferred to 70 per cent to alcohol. By careful manipula-
tion with needles the thick " chorion " can now be removed and the
hardened egg escapes without injury. Eeichenbach was accustomed
to remove the embryonic rudiment from the egg by means of a sharp
knife, then to stain it in picrocarmine, thoroughly dehydrate it and
mount it in Canada-balsam ; and he also studied the eggs by means
of sections cut parallel to and also transverse to the long axis of
the embryonic rudiment.

A ^s^^fe^ B

FIG. 127. — Two sections through the developing egg of Astacus.

(After Morin, from Korschelt and Heider.)

A, stage with few nuclei situated near the ceiitre of the egg. B, stage where tho nuclei have reached
the surface, and the formation of the primary yolk pyramids lias begun, n, nucleus ; y./>, primary
yolk pyramid.

As will transpire immediately, there are many points of the
greatest interest in the development of the crayfish on which
Reichenbach's account throws insufficient light. If, as we hope, this
life -history should become the object of renewed investigation,
the method of imbedding in celloidin and paraffin, described in
Chapter II., would be of the greatest assistance in dealing with eggs
like those of the crayfish, which, owing to the number of yolk grains
they contain, are exceedingly brittle when hardened.

The earliest stages in the development of Astacus were not seen
by Reichenbach, whose work begins with the stage when the nuclei
which result from the division of the zygote nucleus have reached the
surface of the egg, where they form a uniform layer all over its
surface. A Russian naturalist, Morin (1886), has, however, figured
earlier stages, and from him we learn that the zygote nucleus, as in
many other Arthropodan eggs, occupies at first a central position and
divides there ; and that the daughter nuclei are at first internal but
gradually migrate outwards till they reach the surface (Fig. 127).

180

INVEETEBEATA

CHAP.

Eeicheubach found that in the first stage observed by him the egg
was imperfectly divided by radiating planes into a series of radially
arranged pillars, in each of which was contained one of the daughter
nuclei. These pillars were referred to by previous authors as
"primary yolk pyramids." Eeichenbach regards them correctly as
an imperfect division of the egg into columnar blastomeres ; the
cleavage planes which separate adjacent pillars correspond to the
planes which divide adjacent blastomeres in other eggs. He shows,
indeed, that each pillar of yolk is capped on its external surface by
cytoplasm containing a nucleus, and is clothed also on its sides with
cytoplasm.

In Eeichenbach's first stage, then, we have a blastula in which the
blastocoele is filled with unsegmeuted yolk. The yolky part of the
blastomeres, the yolk pyramids, persist as such for a very short time ;
the dividing planes disappear, and we are left with a skin of flattened

cells surrounding an immense mass
of yolk. Such a skin is termed a
" blastoderm."

The formation of the gastrula
is initiated by an increase in num-
ber of the blastoderm cells on one
side of the egg. They press on each
other laterally and become columnar
in character, and so the " ventral-
plate " is formed. This ventral
plate indicates the future neural
side of the embryo. Strictly speak-
ing, all cells within the confines of
the plate have not the columnar
character ; tin's is confined to five
circular areas, in each of which
the cells are arranged in elegant
concentric curves and in lines
Of these five areas the two anterior

and widest apart are termed the " cephalic lobes." They are the rudi-
ments of the paired eyes and of the cerebral ganglia, and in the centre
of each is to be found a pair of cells larger and clearer than the rest.
Behind the cephalic lobes, and situated so close together as almost
to touch one another, are two similar areas, which Eeichenbach terms
the thoracico-abdominal rudiments ; and behind these again, in the
middle line, is a single circular area, the endodermic rudiment. At
the front border of the endodermic rudiment the cells are engaged in
active proliferation, and here they are not in a single layer but in
several layers of small rounded cells. This is the point of origin of
the mesoderm.

In the next stage the areas of the ventral plate which intervene
between the five circular areas shrink so as to bring these latter closer
together. This shrinkage is almost certainly due to a change in form

FIG. 128. — Sagittal section through the
blastula of Astcicus flwinatiMs to show
the primary yolk pyramids. (After
Reiclienbach.)

Letters as in previous figure.

radiating from a central point.

VIII

AKTHKOPODA

181

of the blastodermic cells from a flattened to a more columnar shape.
The cephalic lobes, which have increased in size, are brought nearer
to each other so that they are only separated by a groove, and they are
also approximated to the thoracico-abdominal rudiments. The endo-
derrnic disc is indented in its anterior portion by a deep, semicircular
groove ; this groove is the beginning of the process of gastrulation
(Figs. 129 and 130), and may be termed the endodermic groove.

The mesoderm which lies in front of this consists of a limited
number of large cells termed primary mesoderm, mingled with a
larger number of small cells. The former will give rise to masses
corresponding to the somites of Peripatus, from which the muscles
aud probably the genital organs arise ; the latter constitute Eeichen-
bach's so-called secondary
mesoderm, they wander
widely and occur every-
where between ectoderm
and endoderm, and appear
to give rise to blood and
connective tissue cells.
Keicheubach emphasizes
the fact that these cells
originate both from ecto-

znv

derm and from endoderm,
but it seems probable that
the primary mesoderm has
an endodermic origin, while
the secondary springs from
the ectoderm.

Soon the endodermic
groove becomes a complete
circle and the periphery
of the endodermic disc is

ilivaginated. Just as We FIG. 129. — Ventral view of an eniliryo of Astacus
have found tO be the Case fluviatiiis, the gastrnla stage, iu order to show the

in other eggs, the process
of invagiuation can be
analysed into (a) an in-
crease in the number of cells and (6) an inwardly directed cytotaxis.
The result of this kind of process is that the centre of the eudo-
dermic disc projects for a time as a kind of endodermic button, but
as the process continues this button is also carried inwards, and a
circular blastopore is left where once there was a superficial disc
of eudoderm. The anterior part of the periphery undergoes the
most rapid invagination, and so the endodermic sac projects forward
beneath the thoracico-abdominal rudiments.

These rudiments are now connected with one another by a bridge
of high columnar cells, and each is also connected with the cephalic
lobe of its side by a streak consisting of parallel lines of columnar

ih.ald

ventral plate. (After Reichenbach. )

r.l, cephalic lobe ; inv, invaginated area of lilastoilrrin ;
ili.niiii, thoracico-abdominal thickening.

182

INVEETEBEATA

CHAP.

cells ; but between the cephalic lobes there is still a groove of flattened
indifferent cells. As a result of these changes we have now a heart-
shaped, coherent, ventral plate of columnar cells.

In the next stage the blastopore changes from a circular to

O

mes1

end

FIG. 130. — Sagittal
section through a
portion of the em-
bryo of Astacus
ffuL'iiitilis to show
the invagination of
the endoderraic
rudiment. (After
Reichenbach.)

end, endoderm, the two
references to ami mark
the anterior and posterior
limits of the endodermic
plate; mes, "primary"
mesoilerm ; me.si, second-
ary niesoderni.

long

an elliptical shape, with its long axis coincident with the
axis of the embryo. The thoracico-abdominal rudiments become
thoroughly united with one another in the middle line, and become
arched upwards so as to project over the open blastopore and partially
conceal it from view. Simultaneously the blastopore begins to close

end

mes

prbct

thabd

FIG. 131. — Two sagittal sections through developing eggs of Astacus flumatttis in order
to show the development of the endoderm. (After Reichenbach.)

A, stnge before the closure of the blastopore. B, stage in which the hind-gut lias appeared. Wp,
blastopore ; cml, endodermic sac ; mes, mesoderm ; proi-t, proctodaeum opening by anus ; th.ulnl, rudi-
ments of thorax and abdomen ; i/p2, endodermic cells swelling up to form secondary yolk pyramids.

by the lateral union of its sides, the process beginning in front, and
its hinder border begins to grow forwards and thus assists in the
process of closing.

Eeichenbach's account of this matter and his figures illustrating it
are most unsatisfactory. He denies that the backward growth of the

vm ARTHROPOD A 183

abdominal rudiment has anything to do with the closing of the
blastopore, and his figures show that this is closed by the iinion of
two flat sheets of endoderm cells, uncovered by ectoderm. Now the
lip of the blastopore is a spot where ectoderm passes into endoderm ;
it is difficult to imagine that in the process of closing there is a
dissolution of this continuity, and the suspicion is aroused that if
these stages were worked over by the celloidin- paraffin method
different results would be obtained. In all probability the dissolution
of continuity is due to the method of section cutting.

At this same time the cells which formed the endodermic button
and which now form the floor of the endodermic sac become more
columnar in shape. This increase in size is due to the fact that they
begin actively to ingest the yolk granules ; and they continue to do
so in successive stages till all the yolk granules, which made up the
unsegmented mass in the centre of the egg, are contained in the yolk
cells. The endodermic cells increase enormously in length during
this process and were termed by the earlier authors the secondary
yolk pyramids ; their growth is, however, little advanced in the stage
which we are now discussing.

As the thoracico-abdominal rudiment advances over the blastopore
it becomes obviously bilobed, and in the notch between the lobes is
seen the last rudiment of the blastopore. In front of this, according
to Reichenbach, i.e. in the bridge which connects the two halves of
the rudiment, a new invagination makes its appearance ; it is the
rudiment of the adult intestine or proctodaeum, which opens by the
anus. It is by no means improbable that further investigation
would show that the proctodaeum arises just where the last vestige
of the blastopore disappeared.

At the same time the two cephalic lobes have become connected
in their hinder region by a curved bridge of columnar cells. Tins is
the rudiment of the labrum or upper lip ; behind it, in a slightly
later stage, an invagination appears which will mark the position of
the mouth and of the oesophagus (stomodaeum), but of these
there is, at this period, no trace. In the streaks of cells connecting
the cephalic lobes and thoracico-abdominal rudiments, three outwardly
directed, semicircular thickenings are observable, of which the hinder-
most pair are the furthest advanced. These are the rudiments of the
first three pairs of appendages, viz. the antennules, antennae,
and mandibles of the adult.

The mesoderm when last considered consisted of a small number
of large and of a large number of small cells. In this stage the large
cells form a mass beneath the thoracico-abdominal rudiment, whilst
the smaller have extended and spread all over the surface of the
ventral plate and form special aggregations in the cephalic lobes and
in the lip rudiment.

As the rudiments of the appendages become more marked the
ventral plate continues to shrink in size and takes on an oval outline.
On the median side of each appendage is to be seen a mass of cells

184

INVEKTEBKATA

CHAP.

car

with large clear nuclei ; these are the rudiments of the ganglia of the
nervous system. The first of these pairs of ganglia is connected with
a similar mass of cells which forms a kind of focal line, surrounded by
the concentric parabolic curves of cells which make up the cephalic
lobes. This focal mass of cells is the rudiment of the primary
cerebral ganglion or protocerebrum, to which later the anten-
nulary ganglion or deuterocerebrum adds itself. The two cerebral
ganglia are connected by a bridge in front of the labrum. To the

compound mass on each
side there is added, at
a later period, the an-
tennary ganglion or
tritocerebrum (tr.c,
Fig. 137). The outer
part of the cephalic
lobe gives rise to the
eye - stalk, the ecto-
derm covering which
gives rise to the visual
lhabd cells of the compound
eye ; at its base there
is a deep groove, the
cells lining which, in
later stages, bud off
the cells which form
the optic ganglion.
This groove may be
termed the cerebral
groove.

The mouth has now
made its appearance
as a groove behind
the labrum and leads
into a narrow stomo-
daeum, which descends
vertically towards the endodermic sac but does not yet reach it.
Behind the mouth there is found a median groove of ectoderm
extending backwards between the ganglia of opposite sides. The
cells forming this groove proliferate and form between each pair of
appendages a thickening, two or three cells deep, which later enters
into the formation of the transverse commissures between the
ganglia of the double ventral nerve cord (Fig. 133).

The primary mesoderm forms a compact mass, in which, however,
some indications of a division into segmental masses corresponding
to the appendages are to be seen. This is one of the points on which
a renewed investigation is very desirable, because Reichenbach's
statements on this point have been overlooked by subsequent workers,
and it has been generally assumed that Crustacea are distinguished

FIG. 132. — The "Nauplius" stage in the development of
. I stacus flwoiatilis viewed from the ventral side. (After
Reich enliach.)

an, anus ; aft, rudiment of first antenna ; o«2, rudiment of second
antenna; <•»/•, ridj,'i- marking the first trace of the carapace; c.l,
cephalic lobe ; lab, labrum ; in, mouth ; inn, rudiment of mandible ;
pr.c, protocerebrum ; th.abd, rudiment of thorax and abdomen.

VIII

ARTHEOPODA

185

B

• J'..::-,-.-" ..'

•••"'V'^v:':V"'<%

•-^{••f' Y"!<3*f-:*

com m

from other Arthropoda by the non-segmentation of the rnesoderm
(Balibur, 1880). The anus is still situated on the dorsal aspect of the
thoracico-abdominal rudiment. It is, however, shifted somewhat
forwards as compared with its former position, and will eventually
pass into the terminal notch and so on to the ventral surface of the
abdominal rudiment ; but this does not happen until a later stage
has been reached.

Finally, on the surface of the egg, outside the thoracico-abdominal
rudiment, there is to be seen a semicircular ridge — very faintly
marked. This is the first trace of the head-shield or carapace.
When this stage of development is reached the ectoderm secretes a
thin cuticle which is detached from
the surface of the egg before further
growth occurs, and we may interpret
this as the first moult or ecdysis, and
as marking the completion of a stage
of development.

Now when we survey what is
known of the life - histories of other
Crustacea we find that, in the majority
of Copepoda, Cirripedia, and Ostracoda,
and in the more primitive Phyllopoda
as well as in a few Schizopoda and
Decapoda, the embryo, when it has
attained this stage of development,
bursts the egg-shell and escapes as a
free - swimming larva, to which the
name Nauplius has been given, and FIG.
which is distinguished by possessing a
large upper lip and only three pairs of
appendages. We can scarcely doubt
that the formation and exuviation
of this cuticle in the embryo of
Astacus is a reminiscence of a con-
dition when the embryo, at this stage of development, became
a free-swimming Nauplius larva — and we regard this as one of the
many proofs that the embryonic phase of development is secondarily
derived from the larval, and not vice versa. We therefore term this
stage of development the Nauplius stage.

Following the Nauydius stage a different form of development
begins; the ventral shield, which had been undergoing contraction,
begins to grow vigorously, and in the angle where this shield passes
into the ventral surface of the thoracico-abdominal rudiment there
is found a zone of rapidly growing cells, and as a result of their
activity the point of origin of this rudiment is carried farther hack.
Tims it becomes bent under the ventral shield, just as a crab carries
its abdomen permanently bent underneath it.

Then if we turn our attention to the appendages, we find that the

133. — Three transverse sections
through the developing nerve cord of
Astacusjluviatilis. (After Reichen-
bach.)

conuii, mass of cells derived I'mm ventral
groove destined to form the tr:nis\n>r
commissure ; g, thickening to form one of
the ventral ganglia ; r.ij, ventral groove.

186

INVEETEBEATA

CHAP.

OC

original three
come longer ;

-mx

-mx^
•mxp^

FIG. 134. — Two views of developing eggs of A/i/ui-it*
/li/rintilis seen from the ventral surface. (After
Reich enbach.)

A, stage in which the rudiments of maxillae have appeared,
and in which the caudal fork is visible. B, stage in which the
rudiments of thoracic appendages are appearing, and in which
theabdomen is segmented, nb, abdomen; aft, firstantenna; aft.ij,
antennulary ganglion (deuterocerebrum) ; uf~, second antenna;
car, fold which becomes edge of the carapace; mi«l.f, caudal
fi irk ; c.g, cerebral groove which gives rise to the optic ganglion ;
lull, labrum; inn, rudiment of mandible ; ;«.)•', lirst maxilla;

in r~, second maxilla ;

, first, second, and third

maxillipedes ; <»', eye-stalk; op.gr, optic-ganglion; pr.c, proto-
cerebrum; ret, retinulae of the compound eye; th, rudiments
of thoracic appendages.

have be-
and that
the second, which is the
rudiment of the antenna,
has become bifurcated at
the end, which is an in-
dication of the branching
of the limb into exopo-
dite and endopodite.
Behind the mandible is
the region of the ventral
shield, which owes its
origin to this budding
zone ; on it are to be
found the rudiments of
five new pairs of appen-
dages, viz. those corre-
sponding to the first and
second maxilla and to
the three pairs of maxil-
lipedes. All except the
lirst of these are very
faintly marked indeed.

The thoracico-
abdominal rudiment has
grown in length and has
become marked out into
segments by grooves. On
the dorsal side, just at
its point of origin, there
is seen an ectodermic
thickening. Below this
there is a plate-like mass
of niesoderm, the ends of
which in the next stage
become bent upwards
and attached to the ecto-
derm, so as to enclose a
space which is the cavity
of the heart (H, Fig.
135). In the sides of
this mesodermal mass,
just as in the case of
Peripatus, irregular
cavities appear (pc, Fig.
135). These are the
rudiments of the peri-
cardia] cavity and they

VIII

AETHKOPODA

187

eventually meet above the heart and separate it from the ectoderm.
The primary mesoderm becomes divided into a double series of spheri-
cal masses, one pair corresponding to each of the segments into which
the thoracico-abdommal rudiment is divided. In these somites cavities

FIG. 135. — Transverse section through the region of the heart in an embryo of Astacus
fluviatilis in about the same stage as that represented in Fig. 134 B. (After Retchenbach.)

end.ii, endoderinal plate ; II, heart ; pe, spaces destined to form the pericardium.

appear which represent the coelomic cavities of Peripatus. At the
termination of the thoracico-abdominal rudiment there is a deep in-
dentation and the anus is no longer visible ; in other words, the tail
is divided into two lobes which are termed the tail lobes or caudal
fork. The anus has in fact been pushed forwards till it lies in the

en

FIG. 136. — Longitudinal section through advanced embryo of Axtni-iHsjIin-itittUx

to the sagittal direction but to one side of the middle line. (After Reichenbaoh.)

all. a, abdominal ganglion; cer, cerebral ganglion ; rue., coelomic cavities; C/H/./J, endoderinal pl.-ilc-;
ext.m, extensor muscles ; proct, hind-gut ; stmn, Imv-gut ; th.g, thoracic ganglia ; r.s, vi-ni,r:il sinus.

notch between these lobes, and it then passes on to the ventral
surface by the partial fusion of the two tail lobes above it. Just in
front of these lobes there is a crescentic area of rapidly growing cells.
This is a second budding zone, and it is to its activity that tin1
increased length of the thoracico-abdominal rudiment is due.

188

INVEETEBRATA

CHAP.

In the next stage the yolk has been completely ingested by
the endoderni cells, which have become in consequence very tall and
columnar in shape, and the fold which gives origin to the carapace
is strongly marked. Beneath it there is a deep groove on each side
which gives rise to the branchial cavity of the adult. Five
additional pairs of appendages, the rudiments of the so-called ambu-
latory legs, the pos-
session of which causes
Astacus to be reckoned
as a Decapod, are de-
veloped, and the first
and second maxilla and
the three maxillipedes
have become bifurcated.

oc

pr.c

th

Ki<;. 137. — Advanced embryo of Astacus fl.imatilis
viewed from the ventral side. The alidonicn and
hinder part of the thorax are cut off and spread out
separately. (After Reichenbach.)

ab, abdomen ; lii-.i; rudiment of branchial cavity ; dt.c,
deuterocerebrum ; r.i-, opening of excretory organ ; lull, labrum ;
pr.c, protocerebrum ; tic, eye-stalk ; th, thoracic legs ; th.g,
thoracic ganglia ; tr.r, trirocerebrum.

FIG. 138.— Two ommatidia from
the eye of a newly-hatched
crayfish in longitudinal sec-
tion. (After Reichenbach.)

corn, cornea ; curn.c, corneal cells ;
ci\vx, crystalline cone ; cri/s.c. crys-
talline cone cells ; rh, rliabdome
shimmering through the retiuula ;
jn'i/, pigment cells.

In the basal part of the rudiment of the antenna a sac appears,
which is the rudiment of the excretory organ (ex, Fig. 137). This
sac appears to be similar to one of the coelomic sacs of the abdomen,
to it is added a large ectodermic pocket which forms the thin-walled
ureter.

Soon afterwards the rudiments of the abdominal feet, or pleopods,
make their appearance; and in the bifurcated antennule there is an ecto-
dermic pit to be seen, which is the beginning of the auditory organ.

vm ARTHROPOD A 189

The cephalic lobes now project freely from the surface of the
as the eye-stalks, and the ectoderm cells covering them have become
several layers deep. These ectoderm cells then become arranged iii
radially directed strings, each of which forms an ommatidium or eye
element ; the outermost cells giving rise by their secretion to the
corneal lens, those beneath them to the crystalline cone, whilst
from the innermost cells the retinula is derived (see Figs. 220-222).

The coelomic cavities of the niesoderm disappear as the primary
mesoderm cells form themselves into flexor and extensor muscles
(ext.in, Fig. 136). The arched dorsal region of the egg begins to flatten
in consequence of the gradual digestion and diminution of the masses
of yolk stored up in the endoderm cells. The outer ends of these
cells, in which the nuclei are situated, gradually separate from the
yolky portions. These latter break up into rounded masses and are
gradually digested. The first place where the cytoplasm separates
from the yolk is in the dorsal surface of the mid-gut, just where the
proctodaeum impinges on it. Here a flat stretch of epithelium, the
"endodermal plate," becomes separated from the yolk (enrLp,¥ig. 135).
Soon the rostral spine begins to be differentiated between the anten-
nules in the head region. The gills appear under the brauchiostegite
as outgrowths from the basal joints of the limbs. The two halves of
the caudal fork fuse to form a simple rounded telson. The ectoderm
everywhere sends inwards solid pegs ; they form the supports for
the tendons and ligaments of connective tissue which are formed by
the wandering cells.

The embryo is now ready to break open the egg-shell and enter
upon its free life. For some time the store of yolk in the endoderm
suffices ; but gradually the extreme convexity of the dorsal hump dis-
appears, as the remaining store of yolk is used up, and the endoderm
cells shrink in size. The flaccid endodermic sac becomes indented
by folds, and is gradually fashioned into the complex structure of
tubes known as the adult liver. Its median portion persists as the
adult mid-gut.

Just before the embryo hatches Reichenbach was able to detect
the rudiments, of the genital organs. These appear in the 14th, 15th,
and 16th segments in the dorsal region, and appear to consist of
rounded masses of cells, in each of which a lumen appears. The
masses seem to be arranged metamerically in accordance with the
segments, and at the hinder end of the rudiment of each side there
is to be seen a tube, which is presumably the rudiment of the genital
duct. Reichenbach's imperfect observations, so far as they go, lit in
admirably with Sedgwick's results on Peripatus.

OTHER CRUSTACEA

We shall now take a brief survey of what is known of the
development of other Crustacea, and shall direct our attention to

190

INVEETEBEATA

CHAP.

two points : (1) the mode of formation of layers, i.e. the differentiation
of ectoderm, endoderm, and mesoderm, and (2) the larval history.

an

FIG. 139. — Two sagittal sections through advanced embryos of Astacus fluviatilis.

(After Reicheubach.)

A, stage in which secondary yolk pyramids are complete. B, stage in which the endodermic sac is
divided into lobes— the rudiments of the liver tubes, ab.a, abdominal artery ; aJ,.g, abdominal ganglia
n.g.m, anterior gastric muscle; an, anus (the reference line goes to a point some little distance inside
the proctodaeum) ; cer, cerebral ganglion ; end, endodermic sac (mid-gut); H, heart; hep, liver saccule ;
/'i/i, labrum; in, mouth; p.i/.m, posterior gastric muscle; proct, proctodaeum (hind-gut); r, rostrum'
st.a, sternal artery; stow, stomodaeum (fore-gut); M, telson ; th.alid, thoraoico-abdominal rudiment;
th.g, thoracic ganglia ; op.a, opthalmic artery ; yj#, secondary yolk-pyramid.

FORMATION OF LAYERS

With regard to the first point, all the fragmentary knowledge
which we possess of the early history of other Crustacean eo-ws
seems to show that they agree in all essentials with the ego°of
Astacus as to the mode in which the layers are differentiated. If we

VIII

AKTHROPODA

191

look at the nearer allies of Astacus, we find that in Homarus (the
lobster) the egg is much larger than that of Astacus, owing to the
presence of a larger amount of yolk, and that the endodermic area
is relatively small. The iuvaginated cells form at first a nearly solid
mass projecting into the yolk ; they multiply and spread through the
yolk, ingesting it as they proceed, and a cavity appears in the interior
of the mass filled with disorganized cells. Eventually they reach its

tnv

end

FIG. 140. — Portions of two sagittal sections through developing eggs of
Homarus americanus. (Alter Herrick.j

A, stage in which the endoderm cells form a solid mass. B, stage in which the endndiTiii tflls air
si>r>';iding through the yolk, deij, degenerate remains of more central cells; end, emloderm ; in/o,
cavity of invagination.

surface, and here form an investing layer; thus secondary yolk
pyramids are not formed.

Much the same process occurs in the prawn Palaemon ; but here
the endoclerm cells become detached -from one another and wander
through the yolk and eventually arrange themselves in an epithelial
layer outside it ; when they have reached this position they become
columnar but never attain the length of the endoderm cells in
Astacus. This kind of development seems to be general throughout
the Decapoda.

In Lucifer, however, as we have seen above, Brooks asserts that
the segmentation of the egg is total, that a hollow blastula con-
sisting of relatively few cells is formed, and that an invagination takes

192

INVERTEBKATA

CHAP.

place by which an archenteron is formed which is large and occupies
most of what was the interior of the blastula.

The development of the Schizopod Euphausia, as far as the
gastrula stage, has recently been worked out by Taube (1909).
Here, as in Lucifer, the egg undergoes total segmentation and the
blastomeres are all of nearly the same size. In this way a hollow
blastula is formed. After the 32-cell stage, however, the cells do not
all divide ; two remain undivided, and form the rudiment of the eudo-
derni, and these, at the 112-cell stage, pass into the interior of the

ep

FIG. 141. — Sections through the developing egg of Mi/sis

(After Wasbauiu.)

A, ventral part of egg showing the solid ingrowth of cells which replaces in vacillation. B, trans-
verse section of embryo sin iwing the formation of the epithelium of the mid-gut, end, endoderm ; IKJ/>,
liver saccule ; v.nc, ventral nerve cord.

blastula. The blastopore is surrounded by a ring of special cells,
and of these two are said to give rise to the mesoderm.

In My sis and its allies, and in Amphipoda and Isopoda, in a word
in all the Peracarida, however, the invagiuation is replaced by a solid
ingrowth of endoderm cells, and when these detach themselves and
wander through the yolk, they form an endodermal epithelium, at
first only on the ventral side of the yolk (Fig. 141). Only very
gradually does this epithelium extend so as to enclose the yolk on
the upper side also. In these cases too we have meroblastic seg-
mentation, i.e. the zygote nucleus, whether it is in the interior < if
the egg, as in the Isopoda, or on the surface as in Mi/sis, gives rise to

VIII

AKTHKOPODA

193

daughter nuclei, which form a blastoderm, at first only on the ventral
surface of the egg • only at a later period do cells come to the surface
of the yolk on the dorsal side also.

When we descend to the lower groups of Crustacea we find that
amongst Phyllopoda the development of the Cladoceran genus
Poli/plie nms has recently been worked out by Kiihn (1912). In
fundamental characters it agrees with that of Euphausia ; the egg
undergoes total segmentation. A 2 -cell stage is followed by a
4-cell stage and this by an 8-cell stage in which there are two
tiers of four cells, and in which a segmentation cavity or blastocoele
makes its appearance. The four cells nearer the animal pole of the
egg are larger and clearer than those nearer the vegetative pole, but
the latter contain most of the yolk, and in one of them are embedded
the remains of the sister cells of the egg, i.e. oocytes, which do not
ripen, but serve as nourishment. In the 16-cell stage we get two

B

Fig. 142. — Stages in the development of the egg of Polyphemus pedictdus. (After Kiihn.)
A, passage from 16-cell stage to 30-cell stage, from the side. 13, 118-cell stage, from below. C,
sagittal section through a stage of between 23(3 and 4.32 cells, end, endodermal cells ; gen, cells of genital
rudiment ; mes, mesoderm cells.

tiers of eight cells each, since every cell except one divides by a
meridional cleavage. This exceptional cell is the one of the four
situated in the vegetative half of the egg, which has received the
remains of the nutritive cells. It divides, not meridionally, but into
an upper and a lower cell ; the lower contains the remains of the
nutritive cells, it is the rudiment of the genital organs, and is
termed the generative cell ; the upper is the endoderm cell, and
gives rise to the lining of the mid-gut. At the next period of cleavage
these two cells do not divide, but all the other cells divide each into
an upper and a lower daughter cell (Fig. 142, A). In this way we
get in the animal half of the egg two tiers of eight cells, and in the
lower half of the egg an upper tier of six cells and a lower tier of six
cells. This lower tier lies at the vegetative pole and forms a horse-
shoe-shaped group surrounding the endoderm cell and the generative
cell. There are thus thirty cells in the egg. Shortly after the
endoderm cell divides into right and left halves, thus raising the
number of cells to 31.

VOL. I

o

194 IN VEETEBRATA

CHAP.

At the next period of cleavage the endoclerm cells divide into
upper and lower daughters, and the generative cell divides into
right and left halves, and in this way a 62-cell stage is attained.
The two generative and four endodermic cells do not, however,
divide in the following period of cleavage, so that instead of
124 cells we have only 108 in the next stage. In this stage
the group of endoderrnic and generative cells is surrounded by a
horseshoe - shaped group of six cells, descendants of the similar
group in the 30-cell stage. This group constitutes the mesoderm
(Fig. 142, B). When the endodermal group becomes invaglnated,
as a result of inwardly directed cytotaxis, the rnesoderrn cells are also
invaginated (Fig. 142, 0). Kiihn derives the mesoderui from the
ectoderm because in the 30-cell and 62-cell stages the mother
cells of the mesoderm are cells which give rise also to daughters
which eventually form part of the ectoderm. But this comparison is
misleading and unjust. The wall of the blastula is differentiated into
regions, an eudodermic below, a mesodermic above this, and above this
again an ectodermic. The mere fact, that when the blastular wall
consists of few cells, mesodermic and ectodermic regions happen to
find themselves contiguous to one another so as to be within the
territory of one of the few nuclei, is of no importance. The rnesoderrn
of Polyphemus corresponds in position and origin to that of Astacus.
The early differentiation of the genital rudiment is a coninion feature
in animals of small size and short life-cycle.

About the development of the other division of Pbyllopoda (i.e.
Branchiopoda) very little is known. The egg of Branchipus is stated
to undergo total segmentation, but the inner ends of the blastomeres
are said to coalesce into a yolky mass, on the surface of which is a
blastoderm. Doubt has recently been cast on this statement, and
there is no doubt that it requires reinvestigation.

The development of Copepoda and Cirripedia seems to be funda-
mentally of a similar type. It may be regarded as a modification of
the type described for Astacus, a modification which is produced by
the diminution in absolute size of the egg, due to the smaller adult
size of the species, coupled with the fact that the nucleus and its
daughter nuclei are not diminished in the same proportion as is the
whole egg. Therefore the amount of nuclear matter relative to the
size of the egg is greater in these forms than in Decapoda, and the
nuclei are also far fewer in numbers. The result of this is to produce
a form of segmentation which might be variously described either as
holoblastic or meroblastic, according as one regarded the nucleus
which remains nearer the centre of the egg, as either — (1) the nucleus
of a huge blastomere whose cell territory includes all the egg which is
not marked out into blastoderm, or (2) as a nucleus in unseginented
yolk which has not as yet had its cell protoplasm delimited.

The development of Lepas and its allies has been studied by
Groom (1894), and the development of Lepas in its earlier stages has
been studied in great detail by Bigelow (1902). In this case the mother

VIII

AETHKOPODA

195

nucleus divides three times successively, aud at each division gives
off a daughter which migrates to the surface and segregates round
itself a blastoderm cell, the pre-existing blastoderm cells also dividing
each time. In this way an investment of the yolk by blastoderm
cells is effected. At the fourth cleavage the mother nucleus gives
rise to a primary mesoderm cell in front and then comes to the surface
itself as the first endoderm cell. Subsequently both mesoderm and
endoderm cells divide into right and left halves, and the endoderm
cells withdraw from the surface. This inwardly directed cytotaxis
is the process of gastrulation. The cells bordering the blastopore at
the anterior end bud off cells which sink inwards ; these may be termed
mesectoderm, and they are perhaps equivalent to the secondary
mesoderm of Astacus. A mesodermal band is formed which extends
forwards and upwards, and along its course three outwardly directed
transverse grooves delimit the three pairs of appendages of the

rnesb

FKJ. 143. — Four sagittal sections through the developing eggs of Lepas aiiatifcra in
different stages of development. (After Bigelovv. )

A, 15-cell stage, formation of mesotlerm. B, 10-cell stage, mesoderm formed. C, 02-cell stage,
formation of mesectoderm. L>, 250-cell stage, formation of mesodermic band. '</;>, blastopore ; entl, eudo-
dermal nucleus ; mi1.-.1, mesoderm ; mcs.ect, mesectoderm ; mes.b, mesodermic band ; }<-, second polar body.

Nauplius. The dorsal extension of these appendages is in reality the
same phenomenon as their outward direction in Astacus, and the
apparent difference in direction is due to the smaller quantity of yolk
in the egg of Lepas.

The development of Gopepoda, to judge from the somewhat con-
flicting accounts which we possess, seems to be essentially similar to
that of Lepas.

A renewed study by modern methods of the development of a
primitive form like Brancliipas would throw a flood of light on the
development of Crustacea generally, and perhaps enable us to under-
stand the conflicting accounts given of the development of Copepoda.

LARVAL HISTORY — THE NAUPLIUS

With regard to the larval history, we may take as type the
development of the common fresh-water Copepod Cyclops, of which
various species are found in fresh water all over the world. If females
of Cyclops carrying egg-sacs are isolated and kept in small shallow

196 INVERTEBRATA CHAP.

glass vessels in pond- water with a little pond-weed, they will live
for a considerable time, and the eggs will hatch out into larvae, and
these larvae can be reared through their complete development till
they attain the adult condition.

When the larvae escape from the egg membrane they have an oval
outline, and are provided with a large, swollen, almost square upper
lip and three pairs of appendages. Of these, the first pair are inserted
in front of the lip, and each consists of a single branch divided into
three joints, of which the centre one is the largest. All three carry
long hairs at their ends. The second pair of appendages on each
side consists of a broad basal piece (protopodite) ; it carries a long,
inwardly directed hook, which nearly meets its fellow beneath the lip.
This pair of appendages is postoral. The distal portion of the limb
consists of two branches, an exopodite or outer branch, composed of
a basal piece and four joints, and an endopodite or inner branch, com-
posed of basal piece and two joints. The basal pieces of exopodite
and endopodite are more or less adherent. The third pair of append-
ages are quite similar to the second, but smaller in size ; the proto-
podite is longer in proportion than in the second pair of appendages,
and it has on its inner side a triangular outgrowth, which carries
one or two long, inwardly-directed bristles. This, like the corre-
sponding process on the second appendage, is masticatory in function.
The exopodite and endopodite consist as before of four and two
joints respectively, but the distal joint of the endopodite projects
inwards. These three pairs of appendages are moved by long, back-
wardly-directed muscles, which converge towards and are inserted
in a small area in the dorsal integument.

The mouth leads into a vertical oesophagus which is provided
with constrictor and dilator muscles. This, from its cuticular lining,
is obviously an ectodermal stomodaeuni. It opens into the true
endodermal gut, which runs backwards nearly to the posterior end
of the animal ; here it opens by an orifice, guarded by a sphincter
muscle, into a short proctodaeum lined by cuticle and derived from the
ectoderm. In front of this opening the midgut gives rise to two
ventro-lateral pouches, which have an excretory function and are
filled with granules of uric acid.

In the base of the second pair of appendages is the opening of a
sac which projects backwards at the side of the mouth. This sac, the
antennary sac, is also excretory in nature, and is homologous with
the similarly situated sac in Astacns.

The nervous system consists of a praeoral brain, on which rest two
simple eyes, and a sub-oesophageal ganglion connected with it by a
pair of cords. The nerves for the second and third pair of appendages
are connected with the sub-oesophageal ganglion.

The little larva was baptized Nauplius by Glaus (1858). The
name had been previously employed by the Danish naturalist, 0. F.
Miiller, for a later stage in the development, when four pairs of
appendages were formed ; he imagined this to be an independent

VIII

ARTHROPODA

197

en

•P

organism. When the Nauplius is just hatched it remains still for a
few seconds, until its cuticle hardens and becomes strong enough to
resist the pull of the muscles. Then it starts on its active career,
swimming by a series of darts through the water, each dart being
caused by a synchronous back-
ward blow of all the appendages.
At each blow of the legs the
masticatory hooks seize any food
particles that they may encounter
and drive them into the mouth ;
feeding and swimming are thus
performed by the same move-
ments.

If we compare this larva with
the stage in the development of
Astacus when a cuticle is first
formed, we can see that there is
a fundamental resemblance be-
tween the embryo in one case
and the larva in the other; the
difference between the two being,
first, that the appendages of the
embryo, since they are not func-
tional, are represented by mere
stumps ; and secondly, that the
embryo possesses cephalic lobes,
and the rudiments of compound
eyes, which are absent in the
larva. But the adult Copepod also has no rudiments of compound
eyes, and the origin and significance of the compound eye is still an
unsettled question.

The little creature, as it begins to feed, grows, and, like all Arthro-
poda, can only grow by casting its cuticle. Just like the embryo of
Astacus, there are two growing regions, one at the posterior end of
the animal, which gives rise to a pointed prolongation of the body
equivalent to the thoracico-abdominal rudiment of Astacus, and one
immediately behind the third appendage.

At the end of the first moult the larva passes into what has been
called the Metanauplius condition, when the small rudiments of the
two pairs of maxillae and the so-called maxillipede, or third maxilla,
appear behind the large third appendage. They are concealed by it,
and hence Glaus, in his original communication (1858), came to the
astounding conclusion that not only the adult mandibles but the
two first pairs of maxillae were derived from the division of the third
appendage of the Nauplius. The posterior end of the larva becomes
bilobed, the anus is in the bay thus formed, and just beneath the spot
where the excretory sacs of the gut are situated there are developed
a pair of stumps, which eventually form the first thoracic feet.

an

FIG. 144. — The Nauplius larva of Cyclops
canthocarnoides from the ventral surface.
(After Clans. )

OH, anus ; at1, first antenna; <ii2, second antenna ;
c»7'> endopoclite ; exp, exoporlite ; gut-, Kiiathobase

f8^ anteima: ^.gnathobase of mandible;

lab, labruin ; mn, mandible.

198

INVERTEBRATA

CHAP.

By three successive moults the length of the posterior part of the
body is increased, and at each moult a new pair of stump -like

FIG. 145. — Three stages in the further develop-
ment of the. larva of Cyclops. (After Clans.)

A, stage in which gnathites have appeared. B,
stage in which rudiments of thoracic legs have ap-
peared. C, stage after critical moult. Letters as in
previous figure. In addition, caml.f, caudal fork ; ex,
excretory matter in the walls of the alimentary canal ;
7Mi, first maxilla; m&, second maxilla; mxp, maxilli-
pede ; tlil-*, first, second, third, and fourth thoracic
appendages respectively ; oc, eye.

rudiments of thoracic feet appears.
Then comes a critical moult, at
which the larva changes its whole
appearance and practically attains
the adult form (Fig. 145, C). The
breadth is diminished and the length
increased ; the first appendage has
become many jointed and approxi-
mates in shape to the first antenna
of the adult. The second appendage
loses its masticatory hook and its
endopodite, and has now become

shorter than the first : it becomes the second antenna of the adult.

The third appendage loses everything but the basal joint, and so is

VIII

ARTHROPODA

199

at'

converted into the mandible. The first two pairs of thoracic legs
are each now distinctly divided into two branches, but both exopodite
and endopodite are as yet un-
divided. The bifurcation of the
caudal end has now deepened, so
that the anus is guarded on each
side by a rod-like appendage — one
half of the caudal fork. In the
base of the second maxilla may be
seen the sac-like rudiment of the
shell-gland — the adult excretory
organ, whilst the antennary sac
has disappeared. The thoracico-
abdominal rudiment is now dis-
tinctly divided into segments.

At successive moults additional
joints are added to the first
antenna, the branches of the
thoracic legs become jointed,
and the posterior thoracic legs

B

csp

FIG. 146. — Two types of Nauplius larva.

A, tlie Nauplius larva of Bnun'hii>iix .-.Vi/i/im//* (after Glaus) combined from two liuun's. li, the
Nauplius larva of Lejwts (after Groom). Letters as in pivri'ding figure. In addition, ''.*/'. faudal spine ;
il.t.l', dorso-lateral spine; //•./, frontal filament ; fil, glandular mass in the base of the dorsi.-l.ilri.il
spine; f/H1, gnathobase of antenna ; gii", gnathobase of mandible; ••>•«/, segments Jn tin: tlioracico-
abdominal rudiment of the Nauplius of Braiirfiiptis ; r.N/', the pre-anal spine.

200

INVEKTEBRATA

CHAP.

become first forked, then jointed, and so the adult form is
attained.

Glaus, in the paper cited, has given an interesting sketch of the
differences between Nauplii of different species, and one of the most
interesting facts which he brings out is that in the larvae of
Cyclopsinidae, in which more yolk is contained in the egg, the
masticatory hooks on the second and third appendages are absent,
and the animal at first takes no food.

When we examine the life history of the Phyllopoda, we find
that in the Branchiopoda and in one or two cases amongst the
Cladocera, the young a_nimal enters on its free-swimming existence
as a Nauplius larva. In most Cladocera, however, the whole
development is completed within the egg-shell, and the animal

int

oc

fe Ih

/

FIG. 147. — The " Cypris " larva or Pupa of Lcpas fascicuhms seen from the side.

(After Willemoes-Suhni.)

wlil, adductor muscle of carapace; aft, first antenna; caucl.f, caudal fork; r.r, excretory c.ru;m
(shell-gland); fix, disc for fixation; Jix.gl, fixing gland; ijn., gnathites (i.e. mandible, first maxilla,
second maxilla); int, intestine; in, mouth; lal>, labrum ; oc1, simple eye; oc2, compound eye; th,
thoracic legs.

hatches out with all the adult features already developed. The
Nauplius larva, when it appears, shows the same general features as
the larva of Cyclops, but the upper lip is very long and projects
backwards, covering the ventral surface.

If we turn to the Branchiopoda we find that the Nauplius larva
is characterized by the great development of the post-oral portion of
the body, and by the fact that the third appendages are not forked
(Fig. 146, A). After the first moult, before any more appendages
appear, the post-oral region becomes marked by a series of four or
five transverse grooves, an indication of as many segments, and in
the larva of Apus these are evident when the larva first escapes from
the egg-membrane. Just as in the case of Cyclops so in Apus and
other genera of Branchiopoda there comes a critical moult, at which
antennae and mandibles are reduced to their adult proportions.

The Cladocera are remarkable for retaining throughout life the

VIII

ARTHROPODA

201

forked nature and swimming function of the second antenna, so that
in their case the "critical" character of the moult is reduced to the
loss of the distal joints of the mandible.

The Cirripedia also begin their free life as Nauplius larvae, which
in all essentials, and even in such minute points as the many-jointed
exopodite and feebly-jointed endopodite, agree with the larvae of
Cyclops. They differ in the development of the dorsal integument
into a great triangular shield, with two antero- dorsal horns, the
dorso-lateral spines, and one postero-dorsal horn, the caudal spine,

ter

fix

FIG. 148. — The fixation of the "Cypris" larva of Lepasfascicularis. (After Willemoes-Siihm. )

A, the larva just in the act of ecdysis after fixation. B, the young Barnacle fixed to a piece of dead
shell. Letters as before. In addition, en, carina ; l.nar, valves of larval carapace ; Itli, larval thoracic
appendages being cast off; sc, scutum ; ter, tergum ; th, adult thoracic app.

forming its three angles, and in the possession of a ventrally directed
pre-anal spine. Further, we find in front of the first pair of appen-
dages a pair of flexible antennae, the frontal filaments. As the
larva grows the thoracico- abdominal portion of the body becomes
divided into segments, on which six pairs of bilobed appendages are
successively developed, whilst in the angle between this rudiment
and the head the two pairs of maxillae appear as buds. Beneath the
edges of the dorsal shield the rudiments of the paired eyes appear
as dark areas. Then comes the critical moult, when the second pair
of appendages completely disappears, and the third is reduced to

202

INVERTEBRATA

CHAP.

its basal blade, whilst on the first antenna there is developed a
disc for fixation. A bivalve carapace now appears which replaces
the old three-cornered larval shield, the six pairs of thoracic legs
acquire swimming-hairs and take over the swimming function, the
compound eyes become functional, and the larva has now passed into
what is termed the Pupa stage.

The pupa swims actively about for some time, but it takes no
food. It finally settles on a suitable spot, and attaches itself by the
disc on the first antenna in which a gland with a glutinous secretion
opens ; by the copious effusion of this secretion the larva is attached.
An ecdysis now takes place and, by the preponderant growth of the
skin of the ventral surface, the animal is rotated into a position in
which it may be described as standing on its head. The praeoral

part of the body grows very much
in size and becomes the stalk,
and shelly plates, the scutum,
the tergum, and the carina,
are secreted by the folds of skin
which constitute the carapace ;
these calcareous plates replace
the chitinous shields of the
pupa. In this way the adult
Barnacle condition is attained
(Fig. 148).

In the development of the
parasitic forms like Sacculina,
which draw nourishment from
the blood of their host through
root - like extensions of the
stalk, the Nauplius possesses
no mouth and is fed by the yolk in its endoderm, and the pupa
on fixation amputates the hinder part of the body.

The Ostracoda also enter on their free-life as creatures with the
three appendages of the Nauplius, but the two flaps of skin con-
stituting the bivalve carapace of the adult are already developed, and
the second and third appendages consist of one branch only, the
outer branch or exopodite being lost. The passage into the adult
condition here is so gradual that one cannot speak of a critical moult.
In the development of the carapace and the unforked character of
the second and third appendages we have an anticipation of adult
characters (Fig. 149).

When we turn our attention to the higher Crustacea we find that
the Mysidacea among the Schizopoda and all the Cumacea carry the
eggs in a brood pouch beneath the body of the mother, and from
these eggs young Crustacea hatch out with all the essential features
of the adult. But in the Euphausiadacea among the Schizopoda, and
in some genera at least of the tribe Penaeidea among Decapoda,
to which Lucifer belongs, the young leave the egg membrane as

add

FIG. 149. — The Nauplius larva of Cypris ovum.
(After Clans.)

aili!, adductor muscle of carapace ; at1, first
antenna ; aft, second antenna ; cer, cerebral ganglion ;
int, intestine ; TO?!, mandible ; oc, eye ; st, stomo-
daeum (stomach).

VIII

AETHEOPODA

203

Nauplii, showing, however, the ridge-like rudiments of two or three
pairs of postoral appendages.

In the case of both Eupliausia and Penaeus a succession of moults
leads, as in other Nauplii, to the development of the thoracico-
abdominal rudiment, and to the
appearance in it of ring- like
segments which first appear in the
anterior or thoracic portion. The
appendages belonging to these
segments, which are the maxilli-
pedes, are strongly developed,
especially the first, which has a
long exopodite used in swimming.
A cephalic shield or carapace
makes its appearance as a frill or
fold round the head region, under-
neath which the future paired
eyes appear as dark areas. In
Penaeus the anterior part of this
shield is produced into a sharp
rostral spine.

The larva is now in the stage
known as the Protozoaea (Fig.
150). Its further development
into what is known as a Zoaea
larva involves the growth and
of the abdominal

segmentation

FIG. 150. — The Protozoaea larva of
Nyctlphanes austral is. (After Spence-
Bate. )

Letters as in preceding figure. .»•!, simple
anterior eye ; oc2, compound eye ; th..s, thoracic

portion of the body, the thoracic

segments remaining extremely

narrow, especially the posterior segments.

ones, and the paired eyes become

stalked. In Euphausiadacea the stalks are so short that the paired

eyes do not project beyond the edge of the carapace, and the larva

is consequently known as a Calyptopis. The majority of Decapoda

pass through the Nauplius stage during their embryonic life and

only enter on their larval life as Zoaeae.

ANCESTRAL CRUSTACEAN

We may now pause to consider how far the Nauplius larva may
be regarded as representing an ancestral Crustacean form. Since
it occurs in all the lower groups of Crustacea with no greater
modifications than are found, for instance, in the different types of
larva amongst Echinoidea ; and since it also occurs in isolated cases

.

amongst the higher Crustacea ; and since, furthermore, an embryonic
stage corresponding to the Nauplius is clearly marked in the
development of every Crustacean egg which has been so far studied ;

204 INVERTEBRATA CHAP.

it is quite clear that the common ancestral stock of Crustacea passed
through a larval stage corresponding to the Nauplius.

Now, on the principles laid down in the first chapter of this book,
we are driven to conclude that the Nauplius represents a common
ancestor of all Crustacea in however modified a form. Fritz Miiller,
in his work, Filr Darwin (1864), concluded that all Crustacea were
actually the descendants of a small oval, unsegmented species of
animal with three pairs of legs. Hatschek (1877 and 1878), on the
contrary, pointed out that such a conclusion implied that the Crustacea
had no affinity with Annelida, nor with Peripatus, Arachnida, and
Insecta, in all of which the early embryo was comparatively long
and distinctly segmented, with a double series of ccelomic cavities.
This conclusion Hatschek rightly thought to be incredible, and he
therefore adopted the opposite opinion, namely, that the Nauplius had
no ancestral significance at all, but that since in all Arthropoda — and
Annelida, for that matter — the segments were developed from before
backwards, so that the first was the oldest, there must in all exist a
stage in which there were only three segments in the embryo, and,
according to him, it was due entirely to a secondary modification that
the eggs of some Crustacea were hatched when they reached this stage.

Korschelt and Heider, agreeing in the main with Hatschek,
suggest that the Nauplius is an " Arthropodized Trochophore " —that
it represents the Trochophore of Annelida with certain Arthropodan
features precociously added. Balfour (1880), finally, whilst believing
that the Nauplius in its present form was much modified, yet believed
that it exhibited ancestral features, and that the hinder part of
the body had formerly exhibited a segmentation which it had
secondarily lost.

Amongst all the views we have recounted, that of Balfour seems
to come nearest the truth. It was reserved for his pupil and
successor, Sedgwick, to enunciate clearly what Balfour instinctively
felt, viz. that the embryonic phase is secondarily developed out of
the larval stage, and not vice versa. Indeed, Hatschek's view is
thoroughly inconsistent with the fact that, when the larva does not
hatch out as a Nauplius, a cuticle is produced and shed by the embryo
whilst still within the egg-shell when it reaches the Nauplius stage,
thereby showing that formerly this stage must have been passed
through in the open, in the ancestors of the forms in which it is now
purely embryonic.

We saw in Chapter I. that a larva, as compared with the
actual ancestor which it represented, is usually greatly diminished
in size, and that this diminution in size is not accompanied by a
representation of all the organs which the ancestor possessed, also
diminished to scale, because such diminution would render them
ineffective ; on the contrary, we saw that those organs which were
functionally dominant in the ancestral condition are reproduced by
the larva, while the others are suppressed.

We are, therefore, probably nearest the truth when we suppose

VIII

AETHEOPODA

205

that the Crustacean ancestor was like a Polychaete Annelid, with
fairly numerous segments bearing somewhat feeble and membranous
appendages like parapodia, but possessing greatly enlarged append-
ages attached to the first three segments, which fulfilled the major
part of the work of locomotion, the first pair of these appendages
alone having passed in front of the mouth. Corresponding to the
diminution in size of the whole body in the larva as compared with
its original size in the ancestor, the comparatively functionless
posterior appendages have been suppressed.

But from such a form, with only one pair of appendages in front

u.L

of1

aiudf

caudf

FIG. 151. — Dorsal aiid ventral views of the " Copepodid" larva of Adheres ambloplitis.

(After Wilson. )

A, dorsal view. B, ventral view, afl, first antenna; cii2, second antenna; amd.f, caudal fork;
fr.ijl, frontal gland ; lab, labrum ; mn, mandible ; mx1, first maxilla ; mxz, second maxilla ; •»!.>•/ «, maxilli-
pede ; th, thoracic le^s ; it. I, under lip.

of the mouth, with the two next pairs in the form of powerful
locomotor organs not specialised for either mastication or sensation,
the Araclmida can be derived ; and the fact that Onychophora and
Insecta likewise have only one pair of antennae shows that they too
could be traced back to such an ancestor. Finally, the extinct
Trilobita, whose jaws bear long forked palps, and which possess only
one pair of antennae, seem clearly to belong to the same cycle of affinity.
That this reasoning is justifiable and not far-fetched we may
illustrate by taking a case where we may almost say that the
ancestor is known, and where we are therefore in a position to
compare the ancestor and its representation in the larva. This is
the life-cycle of the parasitic Copepod, Adheres amUoplitis, which

206

INVEETEBEATA

CHAP.

has been worked out by H. Wilsou (1911). The adult lives on the
gills of the rock-bass, Ambloplites rupestris : it is a sac-like organism
fixed by two conjoined arms to the host; it shows no trace of
Copepod structure except the long egg-tubes, which the female bears

protruding from the end of her
body. If we were to classify by
adult structure alone, no one
would dream of regarding Ae-
ther es as a Copepod; but yet
every zoologist is fully convinced
that Adheres is a modified
Copepod — that is to say, that it
is descended from an ancestor
which was like Cyclops or Calanus
or some other typical Copepod

genus.

FIG. 152. — Dorsal and lateral views of just-
fixed female of Adheres ambloma/it.
(After Wilson.)

A, dorsal view. B, lateral view. Letters as in
preceding figure ; fr.f, frontal filament.

Now the Nauplius and Meta-
nauplius stages are completed
inside the egg membrane, and
the young animal hatches out as
what is termed a Copepodid—
namely, in a form wliich every
one would recognize at a glance
as showing the typical structure

of a Copepod, that is, of the ancestor. When, however, we look

closely at this Copepodid larva we find that it differs from an ordinary

Copepod in the following points:— (1) There are but two free

segments in the thorax each carrying

a pair of forked swimming appen-
dages, whereas five such segments on

the normal Copepod carry four pairs

of forked swimming appendages and

one rudimentary pair ; (2) the exo-

podites and endopodites of these legs

are not divided into joints, while the

corresponding members in an ordinary

Copepod are many-jointed ; (3) the

first antennae are short, stumpy, and

lew-jointed, as contrasted with those

in an ordinary Copepod, where they

are normally long and Composed of FKJ. 153. — Lateral view of female

many joints ; (4) the second antennae Adheres amUopiitis after adult
in the Copepodid are likewise exceed- (After walS ) have *"" *^™A'
ingly short, and although forked each Letters as in'preceding flgures_

branch is unjomted and the inner

one terminates in a hook, whereas in the normal Copepod this
hook -like termination is not found; (5) in the jaws, i.e. mandible,
maxillae, and maxillipede, there is nothing which'could be described

VIII

AETHEOPODA

207

at1

mn

as atypical, but a long convoluted glandular tube lies in the mid-
dorsal region of the head and opens at the front end of the carapace,
and this tube secretes a long gelatinous filament.

The larval stage of the Copepodid only lasts thirty-six hours at
most. The larva is swallowed by the rock-bass, and has the instinct
to burrow into the mucous membrane of the pharynx of its host.
When the pointed front end of the carapace of the parasite comes
into contact with the bone of the gill arch of the host, the distal end
of the filament already referred to is extruded from the frontal
gland, and adheres thereto. The larva backs off, and the filament
draws out ; but before it is completely extruded the larva grasps the
end of it by the incurved hooks of the second maxillae, and holds on.

A moult follows, in which the maxillipedes are shifted forward
so that their bases are now
situated between those of
the second maxillae. The
second maxillae are greatly
enlarged, and have lost their
segmentation though their two
incurved ends still tightly
grasp the filament. A sucking-
tube is formed by the union of
a projecting labruni with an

under lip, and inside this are FIG. 154.— Enlarged view of gnathites and lips

the mandibles, though they can offemaec ^biopiitis seen from the

. -f

still be torced out through

, i TJ i ii, V

lateral slits between these lips.

The minute first maxillae are

attached to the sides of the sucking tube, and the two pairs of

antennae are much shortened ; they are reduced in fact to mere

stumps (Fig. 154).

The animal can now stab the vascular gill of its host with its
needle-Like mandibles and suck its blood, and it grows rapidly in
size, moulting frequently. At the first of these moults practically
the adult form is attained, all trace of the thoracic appendages is
lost, and the maxillipedes are transformed into blunt shapeless lobes.
The filament of the female shortens till the claws of the second
maxilla are actually in contact with the skin of the host ; that of the
male, however, remains long, and he appears to crawl around like a
tethered goat until he finds a female ; then he relaxes his hold on
the filament and seizes the female with his claws, and so is in a
position to effect sexual union.

An examination of the differences between the Copepodid larva
and the typical Copepod shows examples of all the changes we
postulated in explaining the Nauplius ; — we have the reduction in
segmentation, and the disappearance of appendages, or rather the
replacement of a homologous series of appendages by a smaller
number of similar ones ; in fact there is a functional rather than

of1fema/Aeffc^f

side. (After Wilson.)

Letters as in preceding figures. In addition,

* u_;> un°ler °ljp_

208

INVEETEBEATA

CHAP.

a proper morphological representation of these in the Copepodid larva.
If, then, it be a sound principle of science to reason from the
known to the unknown, we are justified in regarding the differences
between the known ancestor of Adheres and the larva by which it
is represented, as a means to deduce the unknown ancestor of all
Crustacea from the Nauplius larva, by which we believe that ancestor
to be represented.

A similar problem confronts us when we consider the significance
of the typical larva of the higher Crustacea, the Zoaea. We have
already seen that this larval form develops out of the Nauplius larva in
the Euphausiadacea amongst Schizopoda, and the Penaeidea amongst
Decapoda. But all the Anomura and Brachyura, so far as is known,

begin their free-swimming life
with the Zoaea stage, and
amongst the Macrura this is
true of the Caridea.

All Zoaea larvae agree in
possessing (1) paired stalked
compound eyes, (2) a carapace
which overlaps and conceals
part of the thorax, and (3) a
segmented abdomen. All agree
further in possessing (4) three
pairs of limbs (i.e. mandibles,
and first and second maxillae)
which are thoroughly modified
to form jaws, (5) in having
the first few segments of the
thorax well developed, and
carrying forked limbs termed
maxillipedes on which a large
part of the locomotor function
falls ; and finally they agree
(6) in having the hinder segments of the thorax either entirely
suppressed or very thin, and without appendages or with mere
rudiments of appendages.

But whilst the general features of the Zoaea may be regarded as
constant, its specific features vary from group to group. The Zoaea
of the Euphausiadacea and of the Penaeidea is characterized by
retaining a large forked second antenna like that of the Nauplius,
which assists in swimming.

The Zoaea of Euphausiadacea has one pair only of maxillipedes
well developed, and it has several other well-marked peculiarities :
thus the last pair of abdominal appendages is developed, and the
border of the carapace projects considerably and conceals the short
eye-stalks from view when the larva is seen from above, hence, as
already mentioned, it is termed Calyptopis (Fig. 155).

The Zoaea of the tribe Penaeidea, amongst Decapoda, differ from

FIG. 155. — " Oalyptopis " Zoaea of N
austmlis, lateral view. (After Spence-Bate.)

car, carapace ; Jiep, liver lobules ; oc, compound eye.

VIII

AKTHKOPODA

209

the Calyptopis in having two pairs of maxillipedes developed, and a
rudiment of the third, and in having small rudiments of appendages
even on the thin posterior thoracic segments ; also in having a
median rostral and two postero-lateral spines on the carapace, and
in having long-stalked compound eyes.

FIG. 156. — Zouea of Penaeus, ventral view. (After Clans. )

1'3, first, second, and third maxillipedes ; pi, rudiments of pleopods (i.e. abdominal appendages) ;
r, rostrum ; th, rudiments of hinder appendages of thorax ; ur, uropods (last abdominal appcnda^c'*).

The Zoaea of the shrimps and prawns (i.e. Caridea) agrees with
the Zoaea larva of the Penaeidea in possessing these spines on the
carapace, but it differs from them and agrees with the Zoaea of the
higher Decapoda in two respects ; (1) in having the exopodite of the
second antenna converted into a flat unjointed scale (squame), as in
the adult Decapod, (2) in having the endopodite of this appendage
much shortened so that this limb is no longer locomotor in function.

VOL. i ?

210 INVEETEBEATA

CHAP.

Three pairs of maxillipedes are, however, developed, and on them
consequently devolves the whole function of locomotion. The hinder
segments of the thorax are completely suppressed, and no trace of
appendages is found on the abdomen (Fig. 157).

The Zoaea of the Anonmra is very similar in general appearance to
the Zoaea of Caridea, but it only possesses two pairs of maxillipedes,
and, generally speaking, no trace of the hinder thoracic appendages
is present at birth although they appear after the first moult, and
the rostral spine is always very long and sometimes enormously
elongated. Finally, the Zoaea of the Brachyura, while agreeing in
most points with the Zoaea of the Auomura, differs from it and all
other Zoaeas in possessing a long mid-dorsal spine sloping backwards.

The very same controversy which developed concerning the
meaning of the Nauplius, raged over the significance of the Zoaea.
Some, like Dohin (1870), held it to represent an ancestor of the

FIG. 157.— Zoaea larva of Crangon vulgar is, lateral view. (After Sars.)
Letters as in previous figure.

Schizopoda and Decapoda ; others, like Glaus (1878), pointed out that
such a conclusion would imply that in the ancestral Decapod the
hinder part of the thoracic region was unsegmented, and that these
segments, when they did appear, must have been secondarily inter-
calated. If such reasoning were justified it would sever the hio-her
Crustacea from all connection with the lower Crustacea, for in these
latter the segments follow one another in development in un-
interrupted series from before backwards ; and so the conclusion was
drawn that the Zoaea had no significance whatever.

Balfour then pointed out that in the more primitive types of
Zoaea the posterior thoracic segments, although very thin, are distinctly
present, and therefore surmised that the Zoaea might represent in
a modified form the ancestor of higher Crustacea. On the principles
laid down in this book, we must agree with him. The Zoaea was
clearly a larval form in the life-history of an ancestor common to the
Schizopoda and Decapoda, in a word, we might say, to the primitive
Malacostracan, and therefore represented an ancestor of this Mala-
costracan. But in that case, what stage in the evolution of the

VIII

ABTHKOPODA

211

polychaete worm into the shrimp does the Zoaea represent ?
Obviously one in which (1) the first antenna had become purely
sensory, (2) the second antenna had moved in front of the mouth
and had lost its masticatory function, (3) the mandible had become
purely masticatory, (4) the next two pairs of appendages (maxillae)
had been modified into jaws, (5) the main swimming function had
been thrown on the first two or three appendages of the thorax,
and, (6) compound eyes and a carapace had been developed.

If we read over this list we might conclude that the Phyllopod
genus Apus, if it had possessed better developed antennae, would have
given us a good idea of what the ancestor represented by the Zoaea
looked like. The first two pairs of thoracic appendages of Apus are
developed into long antenna-like organs. All the others, of which

d.lsp

rnxi

Fi«. 158. — Zoaea larva of Porcellane longicornia, after the first moult. (After Sars. )

d.l.sp, dorso-lateral spines of the carapace ; r, enormously elongated rostral spiue ;
th, rudiments of hinder thoracic appendages.

there is a great number, are thin and parapodia-like. These, which
must have existed in the ancestor, are not represented in the Zoaea,
owing doubtless to their physiological unimportance and the diminu-
tion in size of the larva. We cannot, however, well imagine that the
abdomen in the ancestor was devoid of appendages, although it is so
in most Zoaeae. In the Zoaeae of the Penaeidea, indeed, the append-
ages of the last segment are developed, and there are vestiges of
appendages on the other segments of the abdomen.

The abdomen, as a region with peculiar appendages, is character-
istic of the Malacostraca, and the physiological necessity which led
to its evolution can be inferred by watching the way in which it is
used by Zoaeae. Many of these swim on their backs, using the long
spines which project from the carapace as a keel. The maxillipedes
are used as oars, and the abdomen functions as a rudder.

We can now form to ourselves a picture of the course which
evolution followed in transforming the ancestor represented by a

212

INVEETEBEATA

CHAP.

Nauplius into a primitive Crustacean. The second antenna became
gradually shifted forward and lost its masticatory function, while the
third appendage became exclusively masticatory and its distal joints
shrank to an insignificant palp. At this stage of evolution the
animal was assisted in mastication by the modification of the append-
ages of the next two or three segments, which formed maxillae, but
which were never greatly changed from their original parapodia-like
condition.

When these changes had been effected the ancestor was definitely
a Crustacean, and from this level the Ostracoda may well have
branched off. In the Ostracod the number of pairs of maxillae varies
from one to three in different genera, and what in one genus is a
maxilla in a neighbouring genus may be a small thoracic limb.
Swimming is mainly performed by the antennae. Finally, in this
group alone among Crustacea, there are retained throughout life two
pairs of excretory organs, viz., a pair of antennary glands as in the

higher Crustacea, and a pair of maxillary
" shell "-glands as in the lower Crustacea.

The Cladocera also must have branched
off about the same period of evolution from
the common stock, and this is true also- of
some of the Phyllopoda. Those genera,
however, like Apus and Branchipus, in
which the antennae have lost their swim-
ming function, represent the higher stage
of development.

Following the stage of evolution which
we have been discussing, a new stage
supervenes in which the swimming function
began to be handed on to the first thoracic
appendages, while the hinder part of the
body became specialized to form a rudder
by the diminution in size of its appendages.
The Copepoda and Cirripedia seemed

d.sp, median dorsal spine of the to haV6 diverged at thlS poillt. Ill them
carapace ; r, rostrum of carapace ag in faQ Zoaea larva the appendages

deflexed and acting as a frontal . . , ,

spine. oi the hinder segments are suppressed

altogether — a phenomenon doubtless due to

the diminution in size, which affects these Crustacea in the same way
as it affects the larvae. A condition just previous to this stage is also
represented by the Zoaea of Penaeidea and Euphausiadacea, in which
a large portion of the swimming function is still carried out by the
second antenna. But the process of " handing on " the swimming
function to the thoracic appendages, once initiated became progressive,
and soon the second antenna became relieved entirely of its swimming
functions, which were then exclusively performed by the thoracic
appendages, whilst the second antenna was set free for sensory
functions.

FIG. 159. — Zoaea larva of the
Crab Xa,ntho. (After Cano.)

VIII

AETHEOPODA

213

This stage is represented by the Zoaea larvae of Caridea,
Anomura, and Brachyura. The Zoaea is transformed by several
moults; lirst into a Metazoaea, in which the rudiments of the
appendages of the abdomen and of the hinder segments of the
thorax appear; secondly into a so-called "Mysis" stage, in which,
typically, the hinder segments of the thorax bear forked limbs
designed to assist in swimming, and in which the first appendages of
the thorax tend to become somewhat diminished in size and degraded
from the rank of locomotor organs of prime importance to that of
maxillipedes.

This Mysis larva, as its name implies, is of such obvious ancestral
significance that no one has ever attempted to deny that it represents
a Schizopod ancestor. We can, however, even here trace the work

at

FIG. 160. — " Mysis " larva of Homrtrtis mnericanus, lateral view. (After Herrick.)
r.i-'-i'.!1", the seven exopodites borne by seven of the thoracic legs.

of the same modifying tendencies which have, obscured the ancestral
significance of the Nauplius and the Zoaea. In such of the Nephrops-
idea as do not complete their development within the egg-shell (cf.
Ho mar us, the lobster, and Nephrops, the Norway lobster) the larva
emerges in the Mysis condition, with this difference, that the
abdominal appendages are at first quite suppressed.

In the Loricata, of which the rock-crayfish, Pali H in- HA, and the
square-nosed lobster Scyllarus are the best known representatives,
the larva emerges from the egg-shell in a singularly modified Mysis
stage (Fig. 161). In this larva the thorax is broad and flat and of a
glassy transparency ; the abdomen, though distinctly divided into
segments, is very small and has no rudiments of appendages. The
thorax has only six of the eight pairs of appendages which it should
possess if normally developed, and of these, those representing the
first two pairs of maxillipedes are small but those represent ing the
third maxillipede and the first three pairs of walking thoracic

214

INVERTEBKATA

CHAP.

legs, have enormously long endopodites and short outer forks
(exopodites).

Here we see, as has been repeatedly emphasized in this book, that
Nature treats as a single organ an apparatus consisting of several
pairs of metamerically arranged organs, which co-operate in the
performance of a single function ; and when the whole organ is
diminished in size — as when it is reproduced in a larva — the number
of component similar organs is reduced also.

This modified Mysis is known as a Phyllosoma or glass-crab. As

FIG. 161. — "Phyllosoma" larva of Palinurus mil (jar is, ventral view.
(After Cunningham.)

(ili, abdomen ; hep, liver saccules seen through ex, exopoclite of thoracic appendages.

it grows and moults the first maxillipede grows larger, and the last
two pairs of thoracic legs also make their appearance ; so also do the
appendages of the abdomen, and thus the adult condition is approached.
The explanation of the singular appearance of this larva is, that in
the case of the Loricata the Mysis has ceased to be an actively-swim-
ming organism and has become a surface-drifter ; the long legs being
widely spread out and acting as supports.

Another series of modifications of the Mysis stage have been
described by Sars (1891) in the case of the Craugonidae amongst
Caridea. The Zoaea of these forms it will be remembered has,
when hatched, three pairs of maxillipedes developed as forked swim-

VIII

AKTHROPODA

215

ming appendages. In subsequent moults a varying number, but in
no case do all the remaining segments of the thorax develop swimming
appendages. Thus in Crangon only one extra segment develops
forked appendages (Fig. 162), in Cheraphilus two segments develop

at*

FIG. 162. — " Mysis " larva of Crango^ AllTiianni, lateral view. (After Sars.)

M, telson ; exp1'^, the four exopodites borne by the three maxillipedes and great chela respectively ;
pi, pleopods (abdominal appendages); u>; uropods (last abdominal appendage); th*s, the appendages
which will form the five pairs of walking legs.

appendages with exopodites, in Pontophilus two, and in Scibinea one
only. Those segments that do not develop swimming appendages
give rise to simple, unforked appendages, which at the last moult
develop directly into the hinder walking
legs of the adult, as in the case of the
Loricata, and we may add, as in the
case of the Mysis larva which develops
out of the Zoaea larva of Thalassinidae,
another family of the Caridea.

Finally, in the Brachyura all the
thoracic segments behind the first two
which bear the swimming appendages
of the Zoaea, develop only rudimentary
bud-like appendages whilst the larval
swimming stage persists, but when this
is over and the larva begins life at the
bottom, then these appendages develop
directly into the walking legs without
ever passing through a forked stage.

Thus, in the life-history of the crabs
the Mysis stage has been completely
eliminated, but nevertheless the Zoaea
does not change into the adult stage
but into a form called a Megalopa, in
which the carapace is longer than broad, and in which all the seg-
ments of the abdomen possess well-developed swimming appendages.
This larva obviously represents a Macruran stage in the ancestry "I

Fiii. 163. — "Meyalopa" l.'irva of the
Crab I'iliiniiiux, ilorsul view.
(After Cauo.)

Letters as in preceding figures.

216

INVERTEBRATA

CHAP.

crabs, just as clearly as the Mysis larva represents a Schizopod
stage in the ancestry of Macrura. The Megalopa is transformed
into the aduit by one or two moults.

The life -history of the Anomura closely resembles that of the
Brachyura; in their case also the Mysis stage is omitted, but the
third appendage of the thorax, the third maxillipede, becomes func-
tional before the critical
moult which ends the free-
swimming life. The post-
larval stage of the Paguridae
or hermit crabs, which corre-
sponds to the Megalopa stage
of Brachyura, is distinguished
by the possession of a sym-
metrically-developed ab-
domen— an indication that
these asymmetrical forms
are descended from ancestors
which were bilaterally sym-
metrical. It has been found
that the abdomen of the
young Pagurid becomes
asymmetrical before the
animal seizes on an empty
shell in which to shelter its
abdomen. This fact is of
extraordinary interest on
account of its bearing on the
nature of heredity.

The curious groups of
Stomatopoda, which agree
with Schizopoda in having
only three pairs of appendages
modified as jaws, and in

FIG. 164. -Two views of first post-larval stage hJVmg exopodites On 801116

of Eupagurus bernhurdi corresponding to the °* tne thoracic appendages ;

Megalopa stage of Brachyura. (After Sars.) but which differ from them,

A, dorsal view. 13, lateral view, br, branchiae attached and indeed from all Other

to thoracic limbs seen through the carapace ; W ,th* , the TV/To !„ • i j.r

two last pairs of thoracic limbs, reduced in size. ' MalaCOStraca, in having the

first five pairs of thoracic

appendages modified into grasping claws, and in having gills
developed on the abdominal appendages, present a life-history which
affords further confirmation of the laws of larval modification, laws
which have made themselves clear in the course of our study. There
is some reason to believe that the life-history of some Stomatopoda
begins with a Nauplius larva. At any rate Lister (1898) has
captured in the open sea a Metanauplius in which the mandible is
reduced to its blade, and in which the rudiments of the maxillae

VIII

ARTHROPODA

21*7

are developed. This larva is shown to belong to a Stomatopod by
the fact that it possesses already two stalked compound eyes, which
distinguish it from the Metanauplii of all other groups of Crustacea.
It has a triangular carapace resembling that of the Zoaea larva, and
the hinder part of the body is formed of an unsegmented abdomen
terminating in a jointed caudal fork.

The next stage in the life-history which is known is the Erich-
thoidina stage, which Balfour compared to a Zoaea larva. In this stage
the larva has a precisely similar carapace and stalked eyes, but the
first antenna has developed a second flagellum and so become forked,
whilst the second antenna is now unforked. There are the usual
three pairs of jaws, and these are followed by no less than five pairs

mxp~

FIG. 165. — Two stages in the development of a Stomatopod larva.
A. After Lister. B. After Hansen (from Lister).

A, Early " Metananplius " stage. B, So-called " Zoaea " or Erichthoidina stage, d.sp, dorsal spine ;
<7./..s-y. 'lorso-lateral spines ; mxp1'5, the five maxillipedes ; pi, the rudiment of the appendage of the lirst
segment of the abdomen.

of forked swimming appendages. The abdomen is, however, almost
unsegmented, only the first segment with rudiments of its appendages
being present, and it ends like the abdomen of most Zoaeae in a broad
tail-fan. Thus the larva is more like a Mysis larva than a Zoaea, but
differs from both these types of larvae in the character of the abdomen.
In subsequent moults the abdomen becomes segmented and
develops its appendages, whilst the endopodite of the second appendage
of the thorax develops into a great hooked claw, and the first
appendage develops into a long slender unforked limb, the hinder
three pairs of appendages dwindle into insignificant rudiments or
vanish altogether. In this way the Erichthus stage is reached, which
is sometimes termed a Pseudozoaea because it has only the first
two pairs of thoracic appendages well developed, the next three being
represented by mere stumps, and the appendages of the hindermost
thoracic appendages being totally absent. This is transformed into

218

INVERTEBRATA

CHAP.

the adult by a series of moults in which the diminished or vanished
appendages reappear in the form of grasping claws, and in which
the hindermost segments of the thorax develop their appendages
as long legs with the rudiments of exopodites.

In the case of other Stomatopoda the embryo develops within the
egg until it has reached the Pseudozoaea stage ; it then emerges as
an Alima larva, which differs only in unimportant details from the

Pseudozoaea. The
subsequent develop-
ment of the Pseudo-
zoaea is the same as
that of the larva.

Now these life-
histories justify us in
regarding the Stom-
atopoda as derived
from Schizopod ances-
tors, in which the
anterior thoracic
appendages were
gradually converted
into grasping claws
whilst the swimming
function was thrown
on the abdominal
appendages ; just as
we believe that Deca-
poda are derived from
Schizopoda, in which
the posterior thoracic
segments were de-
veloped into ambula-
tory legs whilst the
swimming function is
equally relegated to

the abdomen. The five pairs of grasping claws constitute, from the
point of view of heredity, a single organ which is reproduced in the
Pseudozoaea and Alima larvae as two large functional pairs only.

The Sessile -eyed Decapoda, including Cumacea, Anisopoda,
Amphipoda, and Isopoda, and the division Mysidacea of Schizopoda,
which are all grouped by Caiman (1909) under the name Peracarida,
enter on their free life similar to their parents in all essential features ;
but the just-born young of all these groups agree in having the last
segment of the thorax and its appendages suppressed; another, if
less well-marked, example of the same rule as that exemplified by
the larvae of Stomatopoda.

Amongst the Isopoda, however, there are a considerable number
of genera which have developed suctorial mouths by a union of upper

ur

FIG. 166. — Two later larvae of Stomatopoda. (After Clans.)

A, Pseudozoaea stage of Erichthus Edivartlsi, ventral view.
B, All ma larva of unknown stomatopod. (This larva has moulted
since birth.) In A, in.rp* and mxpr>, rudiments of fourth and fifth
maxillipedes. In B, M6's, rudiments of last thoracic legs ; r,
rostrum.

VIII

ARTHROPODA

219

and under lips, and which become parasitic on other Crustacea.
The shapes of some of these parasitic forms have become distorted
out of all recognition, especially in the female sex. In Portunion
(Fig. lG8),for instance, which belongs to the family of the Entoniscidae,
the " oostegites " of the thoracic legs become enlarged into long leaf-
like folds which are packed together like the leaves in a bud, the
legs themselves having completely disappeared. The head, with its
sucking apparatus, forms a small rounded knob, whilst the abdomen

B

\

Fit;. 167. — Larva and adult female of Pnrtiiiiio/i macnadis. (After Giard.)

A, larva, dorsal view. B, adult female, lab-nil view, abd, abdomen; afl, aiitennule ; "/-, antenna ;
In; brood-sac composed of conjoined ovigerous plates of thorax; g, jaws or gnatliib's ; li, lirad ; /•/,
swimmerets or pli-opods.

is bent back over (not under) the thorax, and its appendages take
the form of crimped laminae.

The larvae of these extraordinary forms have the depressed body
and segmentation of a normal Isopod (Fig. 16*7) : a short pair of first
and a long pair of second antennae, and six pairs of unforked
thoracic legs followed by six pairs of forked abdominal ones. The
jaws are already lancet-like and the lips united. In all but these
last two points they resemble the young of normal Isopoda when
they leave the brood-pouch, and not even the most determined

220

INVEETEBEATA

CHAP.

opponent of the recapitulation theory could deny their ancestral

significance.

It is a tacit assumption of the recapitulation theory that

advance in evolution is corre-
lated with a change in the
environment, and with
consequent acquisition

the
of

new kinds of food by the
animal in the adolescent
stage of its life-history. The
evidence that this theory is
well founded comes out more
and more strongly the more
the embryology of the
various members of the
animal kingdom is studied ;
but i t is exceedingly difficult
to reconcile it with modern
work on the subject of
heredity, which appears to
point to the conclusion that
changes in morphology are
due to changes occurring in
the nuclear matter of the
germ cells before fertilization.
When such chemical changes
have been effected — why, it
may be asked, should their
influence appear just at that
moment of development

when the environment is changed ? Light might be thrown on this
question by a careful and systematic study of the life-histories of
parasitic and abnormal forms, belonging to large families or orders in
the animal kingdom, which show well-established and stereotyped
normal features. Work on these questions will form one of the
most fascinating features of future embryological study.

FIG. 168. — Adult female of Portunwn
with appendages dissected out. (After Giard. )

all, abdomen ; <////!, vestige of first antenna ; nut-,
vestige of second antenna; ceph, swollen head; •;».<;/,
rudiment of maxillipede ; <•/(;>«, the endopodite of the
second abdominal appendage ; enpZ, the endopodite of the
third abdominal appendage ; cost1, the three lobes of
the first oostegite of the right side ; oos/2, the second
oostegite on the right side ; oosfi, the third oostegite on
the right side ; (nwM, the fourth oostegite on the right
side ; oostr>, the fifth oostegite on the right side.

vin ARTHROPOD A 221

AEACHNIDA

Classification adopted—

Delobranchiata Xiphosura
f Scorpionidea

Pedipalpi
Embolobrancniata A

Aranema

l^Acarina
Pentastomida (incertae sedes)

The most primitive Arachnid living is undoubtedly the horse-
shoe crab Limulus, the development of which has been studied by
many authors, but most recently by Kingsley (1892, 1893) and
Kishinouye (1893). The distribution of this genus renders it unsuit-
able as a type of the Arachnida, for it is practically inaccessible
to European students. A similar objection applies to the Scorpion
which, on the whole, must be regarded as the most primitive of exist-
ing land Arachnids ; its absence from the temperate regions of both
hemispheres is a serious drawback, and hence we select our type for
special description from amongst the ubiquitous spiders, and take as
our chief authority Kishinouye (1891-94). This observer has not
only published the most thorough work on the subject but has
examined the course of development in different genera belonging
to different families, and found it identical in all important points.

AGELENA

Amongst the types described by Kishinouye there is one Agelena,
a cellar spider, representative species of which are found all over the
northern hemisphere, and one of which, A. labyrinthica, formed the
subject of an embryological research by the late Prof. Balfour.
Quite recently another author, Kautsch (1909, 1910), has also studied
the development of Agelena labyrinthica. His conclusions in the main
confirm those of Kishinouye, but in some points he has penetrated
further in the analysis of the development of this species than
Kishinouye ; in other points, again, it seems likely that his variations
from Kishinouye's account will turn out to be incorrect. We shall
therefore select Agelena as a type. The species of this genus can
be kept and will breed in captivity. The eggs of Agelena, as of
all spiders, are enclosed in a cocoon of silk ; the mother attaches this
cocoon to a corner of the cage, and in this way eggs of all stages of
development can be obtained.

Kishinouye had also recourse to a "wolf spider," Lycosa, which
spins no web but wanders about in search of prey, and species of this
genus are as widely distributed as those of Agelena. Since Lijcosa
carries about its eggs in a cocoon attached to the underside of its
abdomen, where they remain till the young spiders are hatched,
the later stages in development can always be obtained by capturing

222

INVERTEBEATA

CHAP.

the adult female ; but Lycosa cannot be induced to breed in
captivity.

Kishinouye's method of dealing with the eggs is as follows. The
earlier stages were plunged into water of a temperature of from 70° to
80° C., the later stages were placed in cold water which was gradually
heated to this temperature. When the eggs had become opaque and
white they were removed, and when cool they were placed at once in
70 per cent alcohol. After 24 hours in this reagent, they were
examined under the dissecting microscope and the egg membrane
pricked with a needle, the hardening was then completed in
ascending grades of alcohol. It was found that after staining in
picro-carrniue the paraffin penetrated better than after other stains.
It is clear that the celloidin-paraffin method of embedding would be
more suitable than that of pure paraffin, which Kishinouye employed.

n

FIG. 169. — Three stages in the segmentation of the egg of Ayelena. (After Kishinouye.)

A, stage before the division of the zygote nucleus has taken place, showing the ends of the radiating
columns of the yolk ; B, stage in which the zygote nucleus has divided once; C, stage in which the
zygote nucleus has given rise by repeated divisions to a considerable number of nuclei. n, nuclei
surrounded by islands of cytoplasm ; y.r, yolk rosette.

The egg possesses an inner thin vitelline membrane and an outer
chorion, and the surface of the latter is beset by a mosaic of very
fine granules. At the centre of the egg there is an accumulation of
protoplasm, which contains the zygote nucleus, and is termed by
Kishinouye the centroplasm. There is also, as in all centrolecithal
eggs, an outer rind of protoplasm, which Kishinouye terms the
periplasm (per, Fig. 11). Between the centroplasm and periplasm
the yolk is arranged in a series of radiating columns, each column
consisting of a radiating series of short tangential rows of yolk
granules. Between adjacent columns Kishinouye surmises the
existence of radiating sheets of protoplasm connecting the centroplasm
with the periplasm, but he was not able certainly to demonstrate
their existence.

The periplasm is marked out into polygonal areas which corre-
spond to the yolk columns, and indeed form caps to them. These

VIII

AKTHEOPODA

223

areas cause the egg, when it is newly laid, to appear as if it had
already undergone segmentation, and the whole structure of the egg
at this time irresistibly reminds one of the segmented egg of Astacus
with its primary yolk pyramids. Nevertheless, the resemblance
between the two eggs is purely illusory ; for the egg of the spider
when newly laid contains only one nucleus, and the polygonal areas
seen in the periplasm are due to the pressing of the soft periplasm
against the resisting yolk columns as the egg is squeezed in passing
down through the oviduct.

When the nucleus divides into two the yolk columns become
massed together into two rosette-like bundles, with one nucleus in
the centre of each bundle ; and a small blastocoele appears at the
centre of the egg. The same process is repeated when the next
division takes place, and so there are as many yolk rosettes as nuclei.
In consequence of this rearrangement of the yolk columns they shift
with relation to the
polygonal areas of
the periplasm, and
these latter no longer
form caps to them.
As the nuclei in-
crease in number the
segmentation cavity
enlarges, and the
nuclei gradually
travel towards the

Surface of the e^g

When the number

^f-,^ ,^1™ Vvr> ir>4-t-r>-ii->ns1 A. staije in which the primitive streak and the primitive cumulus are
Ol nUClcl IlabclUlcllIlcll , , „ , . , ., .. , , ...

connected. B, stage in which the connection between the two is broken

oU, all reaCD the SUl'- and the primitive cumulus is migrating backwards (V). (After Kautsch.)

face ; but the multi-
plication of the nuclei still continues, and when 100 nuclei have been
formed the periplasm becomes completely separated from the yolk and
transformed into a blastoderm of rounded cells.

The blastocoele seems by this time to have disappeared. As the
blastodermic cells multiply they become more flattened, except at
one spot, which Kishinouye names the primitive ventral thickening
and which we may term the primitive streak. Here the blastoderm
cells remain rounded; they proliferate cells into the interior of the
egg, and thus initiate the gastrula stage and the formation of layers.
The primitive streak becomes elongated, and at one end of it another
thickening appears, caused also by the cells of the blastoderm retaining
a rounded shape and proliferating inwards.

What the meaning of this secondary thickening is Kishinouye
could not ascertain, because he could not 'determine whether the side
of the primary thickening, where the secondary thickening appeared,
was anterior or posterior ; it appears probable, from what occurs in
the development of other Arachnida, that this secondary thickening

Fiu. 170. — Surface views of the developing egg of Agelena
labyrinthica, showing the primitive streak and the primitive
cumulus. (After Kautsch. )

224 INVEKTEBKATA CHAP.

is the primitive cumulus, and that it appears at the hinder end of
the primitive streak. Amongst the cells budded off from the primitive
cumulus are probably the mother cells of the genital organs. It
should be noted, however that Kautsch regards the so-called primitive
cumulus as a thickening of no special significance, and expressly
denies that it has anything to do with the genital organs — he re-
gards it as separated from the front end of the primitive streak.
The difficulty is that it has ceased to be recognizable before the first
traces of segments have appeared in the embryo, before it has become
possible to determine the long axis of the embryo with certainty.

After the secondary thickening has disappeared as a distinct mark,
the primary thickening extends so as to form, when seen from the
surface, an oval plate, which may be termed the ventral plate, on
which the first rudiments of the future organs make their appear-
ance. Transverse sections show that the proliferations of cells from
the primary thickening form a longitudinal keel-like ridge projecting

into the yolk. This
mes. keel -like ridge re-

presents a solid in-
vagination of eudo-
derrn. From the
edge of the keel, cells

ffi/$~^ are given off which

j wander through the

yolk, increasing in

FIG. 171. — Section through the primitive streak of Age/end to •'. , °

illustrate the formation of the germ layers. (After Kishinouye.) Slze as tney d.0 SO,

and they eventually

1'inl, endoderm ; mes, mesoderm. TT i -j-i

establish an epithe-
lium on the outer surface of the yolk in the manner described below.
These cells constitute the permanent endoderm. The rest of the ridge
flattens out laterally and becomes divided into two parallel bands lying
beneath the ectoderm; they constitute the mesoderm (Fig. 170).

Soon, as seen from the surface, the ventral plate becomes crossed
by transverse grooves, which are the first indication of a division of
the animal into metamerically arranged segments. In front there is
an undivided cephalic lobe ; behind, a caudal lobe ; and the inter-
vening plate is divided, in the earliest stage observed by Kishinouye,
into five segments. Of these, the first corresponds to the segment
from which the second pair of appendages, the pedi palpi, develop;
the others correspond to the segments which bear the walking legs.
The segment which gives rise to the first appendages or chelicerae
develops later, being cut out from the cephalic lobe.

As development proceeds, further segments are cut out from the
caudal lobe, till a total number of ten abdominal segments has
appeared. The mesodermic bands have meanwhile undergone a
corresponding segmentation into squarish blocks of cells, the somites,
in each of which a coelomic cavity occurs. The tenth segment is not
always distinct, nor does its somite always develop a cavity. Soon the

VIII

ARTHROPODA

225

rudiments of appendages appear as paired outgrowths from the seg-
ments, developing in order from before backwards, and a pouch from
the corresponding coelomic sac extends into each of them.

The abdominal appendages grow slowly and only form rounded
knobs ; they do not grow nearly as quickly as the appendages on the
other segments, and are absent on the seventh to tenth abdominal

O *

segments. The first abdominal segment gradually disappears ; it
possesses indications of a pair of appendages, but they never develop
beyond the condition of slight elevations and soon disappear altogether.
Very occasionally indications of a pair of appendages are found on
the sixth segment. These also soon disappear.

The cephalic lobe, the origin of which has already been described,
becomes divided into two semicircular lobes, in each of which a
semicircular groove -like invagination is formed, which is almost

Fiu. 172. — Two views of embryos of Agelena at the period of maxima fti extension of the
ventral plate (i.e. before reversion has begun). The coelomic cavities are seen by their
degree of transparence, and are represented by lighter shading. (After Kishinouye. )

A, lateral view of an embryo. B, dorsal view of a slightly older embryo than that represented in
A. aM5, the abdominal appendages belonging to fourth and fifth abdominal segments ; c.gr, cerebral
groove ; ch, rudiment of chelicera ; c.l, caudal lobe ; coe1'15, the coelomic sacs, from coe1, the sac in the
prae-oral lobe, to coe15, the sac in the seventh abdominal segment ; P~4, rudiments of the legs ; i»:<l,
rudiment of the pedipalp ; stem, stomodaeum.

certainly homologous to some extent with the " cerebral grooves " of
Peripetias and Astacus. This invagination is the chief source of the
cells of the brain ; but there are also formed two invaginations at the
posterior lateral border of the cephalic lobe, which become closed from
the exterior and form little vesicles, and they also contribute to the
building up of the brain. The rest of the nervous system appears
as a series of paired thickenings of the ectoderm near the mid- ventral
line, one pair appearing in each segment. The thickening in each
segment is, however, only a more prominent portion of a continuous
ridge-like thickening which extends through the whole length of the
ventral plate and is continuous with the thickening which forms
one side of the brain.

The stomodaeum is now formed as an invagination just behind
the cephalic lobes but in front of the chelicerae, and the proctodaeum

VOL. i Q

226

INVEKTEBKATA

CHAP.

Wped

appears considerably later, just in front of the tail-lobe, as a similar
invagination.

When we compare the development so far recorded with that of
Peripatus we must be struck with the fundamental resemblance.
If, when the yolky endoderm cells of Peripatus have become invested
by the ectoderm, the gut-cavity — which, it must be remembered, is
formed by a process of secondary absorption — did not appear, then

we should have a solid yolky
endoderm, such as, to judge
from the few observations that
have been made on the subject,
in point of fact appears to exist
in Peripatus novae - zelandiae.
(Sheldon, 1888, 1889.)

The origin of the rnesoderm
as a pair of bands which become
divided into somites, each con-
taining a coelomic cavity, and
the origin of the whole central
nervous system as two ridges
united in front of the mouth in
the region of brain, and behind
the position where the anus
appears as an anal ganglion, is
essentially the same both in the
Spider and Peripatus. In the
cephalic lobe of the Spider on
each side there is a faint split in
the mesoderm, which seems to be
the rudiment of a coelomic cavity.
Whilst all this development
has been going on, the ventral
plate has grown in length till it
almost encircles the ovum, the
part of the circumference which
represents the dorsal surface
being of very small extent, and
the caudal and cephalic lobes
almost touching one another. Underneath this small dorsal surface
there appear at the same time a number of cells gorged with yolk
(" fat " cells). Previous observers had interpreted these to be wander-
ing mesoderm cells and the forerunners of blood corpuscles, but
Kishinouye interprets them as endoderm cells now for the first time
reaching the dorsal surface of the yolk, though he admits that they
develop into the first blood cells. Kautsch points out that at no
time is it possible to discriminate sharply between mesoderm cells
and. yolk cells, since all intermediate stages between these two types
occur.

FIG. 173. — Two sagittal sections through em-
liryos of Agelcna of different ages, but
previous to reversion. (After Kishinouye. )

A, younger stage. B, older stage. Letters as
in previous figure, e.coe, cephalic coelom. In A
no coelomic sacs have appeared in the cephalic lobe
or in the cheliceral segment. In B the vestige of
an appendage on the sixth abdominal segment
present in A has disappeared.

VIII

AKTHKOPODA

227

During the period of development which succeeds the one which
we have just described, a process termed "reversion" takes place.
This consists in the development of the dorsal surface, which now
begins to grow more quickly than the ventral one, forcing asunder

FIG. 174. — A portion of a sagittal section of .[f/r/i'/ni /<//</// -ht/li ii'n, greatly enlarged.

(After Kautseh.)

c.coe, coeloinic sac in cephalic lobe ; c.gr, cerebral groove ; <:l, eamlal lobe ; <l, dorsal siirl'.-iri. :
/.<_-, fat-cells ; 0-10, the coeloinic sacs in the abdominal segments 0-10.

the head and tail lobes, and at the same time forcing the mass of
yolk which occupies the interior of the egg downwards between the
two mesodermic bands. As a consequence, these bands, and the
overlying ectodermic thickenings which constitute the rudiments of
the right and left portions of the nerve cord, become widely separated

ck

ccoe

coe

a

FIG. 175. — Two views of embryos of Agdcna undergoing reversion. (After Kishinouye.)

A, an early stage of reversion. B, a later stage of reversion. nV-, "''•"'. the second and tifUi
rudimentary abdominal appendages. Other letters as before.

from one another, and the very narrow band of ectoderm which
occupies the mid-ventral line between corresponding thickenings of
the right and left sides becomes enormously stretched.

This process is one for which it is very difficult to find a
mechanical explanation. Mere preponderant growth of the dorsal
surface will not account for it. This by itself would only lead to the

228

INVEKTEBBATA

CHAP.

rucking up of the representative of the dorsal surface into an out-
standing fold, just as the growth of the endodermic rudiment in the
pathological blastulae of Echinus, produced by rearing the eggs in
warm water, leads to the formation of a gut rudiment which projects
from the surface of the blastula like the finger of a glove. Another
suggested explanation of reversion is that it is conditioned by the
pressure exerted on the egg by the tough chorion. The peculiarity
about the process is that whilst the dorsal surface increases in extent
it continues to form a part of the spherical surface of the egg ; nay
more, as it extends laterally it actually burrows under the mass of cells
which form the origin of the caudal lobe, and causes this structure to
appear as an outstanding projection. Kautsch points out, however,
that if reversion is to be attributed to the increase in length of the
dorsal surface of the embryo, the dorsal ectoderm cells should be under

cox

FIG. 176. — Transverse sections through two stages
in the development of the heart of Ayelena
labyrinthica. (After Kautsch.)

card, thickened wall of apex of coelomic sac which
forms wall of heart (the reference line is a little too
short) ; H, heart-cavity.

FIG. 177. — The embryo of Agelena
when reversion is complete. (After
Kishinouye.)

co.r, coxal gland ; ster, stercoral pocket ; sp,
spinnerets. Other letters as before.

lateral pressure and should assume a columnar shape, whereas they
are obviously passively stretched since they are exceedingly attenu-
ated. He concludes that no mere mechanical explanation of reversion
is possible.

During the progress of reversion many changes take place. The
first abdominal segment, as well as the sixth, seventh, and eighth,
have by this time disappeared. The coelomic sacs of the abdominal
region extend dorsally till they meet one another in the mid-dorsal
line. Below this point they do not meet, and so a space is enclosed
between their dorsal apices which is the cavity of the heart. In this
space are found many of the " fat " endoderm cells, alluded to above,
which thus form the first blood corpuscles. The walls of the heart
are formed by specially thickened regions of the walls of the coelomic
sacs (card, Fig. 176). Since the coelomic sacs do not fuse with their
successors, there occur gaps in the heart-wall between two segments.

vm ARTHEOPODA 229

These gaps are the origins of the ostia of the heart. The coeloniic
sacs belonging to the cephalic lobe also grow in a dorsal direction.
They then become divided into dorsal and ventral portions. The
latter lose their cavities and disappear, being probably transformed
into connective tissue. The former meet in the mid-dorsal line and
enclose between them a space which forms the dorsal aorta.

The coelomic cavities belonging to the six segments of the
prosoma do not grow dorsally but extend further and further into the
appendages, as these grow longer and become divided into joints.
Soon the greater part of the cavities which are contained in the
appendages disappear, their walls becoming converted into the
extensor and flexor muscles which move each segment of the limb.
The coelom disappears entirely in the segments belonging to the
chelicerae and pedipalpi, but in the four segments which bear the
ambulatory legs a small remnant persists in the base of each leg as a
tiny vesicle. That portion of the coelom which is situated in the

o

gon

FIG. 178. — Longitudinal section through part of the abdomen of Agelena labyrintMca,
in order to show the origin of the genital organs. (After Kautsch.)

3, 4, and 5, the coelomic sacs of abdominal segments 3, 4, and 5 ; gon, rudiment of genital organ ;
c.ii, thickened ectoderm which gives rise to the ventral nerve cord.

base of the first leg becomes connected with an ectodermic invagina-
tion which grows in to meet it. This invagination forms the duct of
the coxal gland ; the glandular portion of the organ is formed by the
union on each side of all the coelomic sacs belonging to the four
walking legs. This excretory organ may therefore be compared to
one of the coelomiducts or so-called " nephridia " of P&ripatus. The
coelomic sacs which were situated in the first abdominal segment
disappear ; those which existed in the sixth, seventh, and eighth
segments fuse into a single cavity on each side, which becomes
pressed into the caudal lobe by the same force which presses the yolk
mass downwards.

The genital organs make their appearance as large pale cells in
the walls of the coelomic sacs of the third, fourth, and fifth abdominal
segments (Fig. 178). When the cavities of these sacs disappear
these cells coalesce to form a compact mass on either side of the body
which is the rudiment of the genital organ. The genital duct is
formed by an outgrowth from the sac of the second abdominal segment
and therefore, like the duct of the coxal gland, it is a coelouiiduct.

230

INVEBTEBKATA

CHAP.

The development of the genital organs of the spider bears a striking
resemblance to their development in Astacus.

In the caudal lobe the first trace of the mid-gut now appears.
An accumulation of yolk cells in the shape of a plate is formed. This
plate becomes bent into a U-shape so as to enclose a cavity which is
the rudiment of the stercoral pocket of the spider. Towards the
main mass of yolk the stercoral pocket is closed by an accumulation
of yolk cells. In this accumulation a cavity appears which develops
into the hinder portion of the mid-gut, and which is, so to speak, a
forward extension of the stercoral pocket. As it grows in length
the stercoral pocket is pushed backwards. From the pocket itself
two lateral outgrowths are given off which form the so-called
Malpighian tubes, the excretory organs which the spider possesses

CK
$

m^ sfer

map

FIG. 179. — Two sections through the developing stercoral pocket and Malpighian tubes
of Agelena labyrinthica. (After Kautsch.)

A, the posterior section. B, the anterior section, map, rudiment of Malpighian tube ;
filer, rudiment of stercoral pocket.

in addition to the coxal gland (Figs. 179 and 180). The ectoderm of
the ventral face of the caudal lobe is thickened so as to form the
so-called anal ganglia, which arise at the posterior point of union
of the two longitudinal rudiments of the nervous system. Just in
front of this point the proctodaeum appears as an ectodermal in-
vagination, and this iuvagination soon afterwards will open into the
stercoral pocket.

The persisting abdominal appendages now undergo further
changes. On the posterior aspect of the first two pairs, near their
bases, an ectoderinic iuvagination is formed. In the case of the first
pair this invagination forms the lung sac. This appendage develops
on its upper and posterior face outstanding folds which are the
rudiments of the first lung-lamellae. The other lamellae of the lung
are formed by outgrowths from the thickened ventral wall of the
lung sac — or to put it in another way, from the basal portion of the
appendage. The credit of having given the first clear account of

VIII

AETHKOPODA

231

the development of the lung is due to Parcel! (1909), whose account

in all essential features

has been confirmed by

Kautsch (Fig. 181). In

the case of the second

pair of legs the invagiua-

tion gives rise to the

lateral trachea. The

median trachea arises as

a modification of the

entopophysis or ecto-

dermal tendon of the

longitudinal abdominal

muscle. The first two

persisting abdominal

segments are very broad,

and hence the hinder

segments are forced back

to near the posterior

end of the abdomen.

The two hinder pairs of

abdominal appendages

become the spinnerets

and in each a solid ecto-

dermic invagination is

formed at the apex of

the limb, and gives rise

to the spinning glands.

muse

dm.

'USC

FIG. ISO. — Sagittal section through the hinder part of
the abdomen of Agdena, lahi/rinthica to show the
hinder part of the mid-gut developing in connection
with the stercoral pocket. (After Kautsch.)

d.Miixc, dorsal longitudinal muscles ; m.g, rudiment of hinder
part of mid-gut; sp, spinneret; sp.gl, spinning gland;
ventral longitudinal muscles.

The third pair of spin-
nerets are formed by the division of an inner lobe from the main

mass of the last pair of
abdominal appendages.
They appear after birth
(Fig. 182, C).

The cephalic lobes
have now fused in the
middle line, and their
semicircular grooves
have also fused at one

•coe

eve2

FIG. 181. — Longitudinal section through the abdominal
appendages of an embryo of Ayelena labyrinth ini,
to show the origin of the lung book. (After
Kautsch.)

abl, ab-, u&3, the first, second, and third abdominal appen-

grooves

point. These
now begin to be closed
in from the exterior,
and the last portions to
remain open are the

dages respectively ; coel, coe^, coeS, the coelouiic sacs belonging lllOSt posterior pai'tS of
to the tirst three abdominal segments; /./, lung lamellae; l.s, fligiv inner lilllbs JtlSt
lung sac.

above the spots where
these grooves finally close, a pair of ectodermic invaginations mark

232

INVEETEBEATA

CHAP.

the site of the central eyes. The lateral eyes are formed as
depressed circular areas iii the ectoderm, one on each side of the
head, i.e. at the edges of the ventral plate. The lateral vesicles are
now completely cut off from the exterior, and Kishinouye compares
them to the eyes of Peripatus.

The chelicerae have been shifted forward so that their bases
nearly meet in the mid-ventral line in front of the mouth, and their
ganglia form the commissure which connects the brain with the large
suboesophageal ganglion. The latter is formed from the ganglia
of the pedipalps and the four ambulatory limbs ; these ganglia are in
close contact with one another, but at this stage have not yet fused.

The above concludes the account of the changes which take place
during the process of reversion. When this process is complete the
undigested yolk forms a huge semicircular protrusion on the ventral

ab

prod

FIG. 182. — Surface views of the cut-off abdomen of three embryos of Agele na

of different ages in order to show the modifications undergone by the abdominal
appendages. (After Kautsch.)

al>--alp, the abdominal appendages ; ab5 (on the right side of Fig. C), the inner part of the last
abdominal appendage, which gives rise to the third spinneret; f.l, caudal lobe; H, the last leg ; jn-oct,
proctodaeal invagination : tr, invagination to form the trachea.

surface, and the mesodermic bands are situated somewhere about the
equator of the egg, which still retains its spherical form.

In the succeeding period of development, which lasts until birth,
the yolk becomes absorbed, and as it disappears the ventral
ectoderm contracts in width, and the two halves of the nerve cord
and the two mesodermic bands approach one another once more. At
the same time the ventral ectoderm grows in length and forms a deep
inwardly directed fold which is the beginning of the constriction
separating abdomen and prosoma from one another. During this
period the various organs complete their development.

We may commence by the consideration of the central nervous
system and eyes. The grooves in the brain become now completely
closed off from the exterior and form crescentic tubes. The inner
portions of these crescentic tubes completely fuse with one another
so as to form the stem of a T, the transverse arms of which are

VIII

ABTHROPODA

233

oc.

formed by the outer portions of the grooves. The walls of the tubes
form the substance of the brain, and this organ shows a distinct
division into three segments. Of these the most anterior is formed
from the cross beam of the T, the other two form the main stem.

The central eyes arise as pits just behind the posterior ends of the
brain grooves, they belong, therefore, to the hindermost segment,
while the lateral eyes are situated even still further behind this
point. Patten's attempt to show that
a pair of eyes belong to each segment
is, therefore, unjustified.

The terms anterior and posterior
must be used with reference to the
mutual positions of the segments as
they lie in the anterior portion of the
ventral plate. By the growth in length
of the ventral ectoderm the segments
become pushed up round the anterior
end of the animal on to its dorsal surface,
so that what was anterior on the ventral
surface becomes posterior on the dorsal.
Thus the median eyes attain a position
behind the lateral eyes, although the
latter are morphologically posterior to
them.

The lateral eyes on each side
originate as a simple ring-like pit of
ectoderm which becomes divided by the

continuance of the process of invagina- FIG> 183 _The condition of tlie
tiou into several deeper secondary pits, brain in the embryo of .•!</>/>/«'

and each of these becomes Closed Off after reversion has taken place.

from the exterior by the constriction ( After Kishinouye.)

Of its Opening. The floors of these A, frontal section of the brain and

. & . , , adjacent structures. B, diagram ot the

Secondary pits are directly Converted brain ; 1, 2, 3, the three segments of the

into retinulae, their component Cells brain ; e.grr, cephalic groove (now closed

becoming visual cells. Between the
upper ends of the visual cells, rhabdorues of cen'trai'eye.
or visual rods are formed, whilst their

lower ends are directly converted into nerve fibres which become
connected with the brain. The roofs of these pits are formed by over-
folding of the ectoderm, and constitute the vitelligenous cells which
secrete the crystalline bodies between them, whilst over all the
general cuticle is continued. The cuticle, which is of course secreted
by the ectoderm, is thickened where it covers the eye, forming there
a lens.

The central eyes have a different fate. When the vesicles out of
which they develop become closed, the last trace of the opening of
each vesicle is situated posteriorly, and each vesicle, therefore, consists
of an upper and an under wall with a slit-like cavity between them.

to form a tube); ch.g, cheliceral
lion ; I. v, lateral vesicle; o.c, rudiment

234

INVERTEBRATA

CHAP.

From the upper, not the lower of these two layers, the visual cells
are developed, and from the ectoderm which covers the whole sac, the
vitelligenous cells are formed. It follows that what were originally
the outer ends of the visual cells are turned away from the light,

£r3

FIG. 184. — Sections through the developing eyes of Aydena. (After Kishinouye.)

A, section through early stage of development of the median eye. B, section through later stage of
development of median eye. C, section through iuvagination from which the lateral eyes develop.
6r;!, third lobe of the brain ; ch.g, cheliceral ganglion ; •»./, nerve fibres ; oc, rudiment of median eye ;
oc.l, rudiment of one of the lateral eyes ; ji.r, post-retinal layer of cells ; r, layer of visual cells ; /•//,
vitelligenous layer.

whilst their basal ends, from which the nerve fibres spring, are turned
inwards. The lower end of the sac forms the post-retinal layer Q>.r,
Fig. 184).

The nervous system before and during reversion is in the form
of a thickening of the ectoderm ; it now becomes detached from the

end

H

stem

"hep

prod

ster

FIG. 185. — Two sagittal sections through embryos of the spider Theridlon •maculufitni, in
two succeeding stages of development. (After Morin, from Korschelt and Heider. )

A, ventral nerve cord, showing ganglia. B, ventral ganglia fused to form a suboesophageal mass.
br, brain ; ilil, dilator muscle of " stomach " (i.e. stomodaeum) : end, endodermic epithelium beginning
to cover the mass of yolk ; //, heart ; heji, liver ; jiroct, proctodaeum ; sb.o, suboesophageal ganglion ; ster,
stercoral pocket ; xfom. stomodaeum or stomach ; r.</, ganglia of the ventral nerve cord.

ectoderm and the ganglia of the ventral chain soon fuse into one
suboesophageal mass (Fig. 185, B). The characteristic poison gland
is developed as an ectodermal ingrowth in the base of the chelicera.
The stomodaeum develops rapidly, sloping upwards and backwards.

VIII

AKTHROPODA

235

Its innermost portion enlarges to form the so-called stomach, whilst
its outer portion forms the pharynx and has its cuticular lining
produced into parallel ridges. The oesophagus is the narrow portion
connecting the pharynx and stomach. At the hinder end of the
stomach an accumulation of endoderm cells is found abutting on
the yolk, which now becomes indented by the ingrowth of four pairs
of mesoderinic septa, and the yolk lobes thus outlined eventually form
the lobes of the liver. These septa seem to be the outgrowths
from the abdominal coelomic sacs, whose cavities have disappeared.
Kautsch maintains

that the epithelium cover- ^"

ing the lobes of the liver
is derived from the meso-
dermic cells of these septa.
This is excessively un-
likely, and Kishinouye's
statement that it isderived
from the anterior accumu-
lation of "yolk cells"
situated where the endo- ^
derm abuts on the yolk, "-eP
and which, according to
him, gradually spread
throughout it and rise to
the surface, is infinitely
more likely. In Astacus
we have already learnt
that the liver lobes arise as
a result of the indentation
of the yolkv endodermic

V f

sac by mesodermic septa,
but in that animal there
is no question that the
epithelium of the liver
arises from the endodermic
nuclei and their surround-
ing cytoplasm, and this is also probably the case in the spider. The
appearance of the lumen of the mid-gut first in the region of the
stercoral pocket is paralleled in Axi/wns by the first appearance of
a definite " endodermal plate " in the hinder region of the mid-gut.

The development of the embryo is now complete and it is
hatched.

nig.

ster

FKI. 186. — Horizontal section through abdomen of an
advanced embryo of A ijelcna labyri iithica to show
the division of the yolk into lobes by septa. (After
Kautsch. )

//, heart ; m.;/, hinder part of mid-^nt ; «v, mesodermic
septa dividing the yolk ; xt> / , sti'iroral pncket.

OTHER AEACHNIDA

What is known of the development of other Araclmida demon-
strates that it is in remarkable agreement with that of the spider,
in all essentials, but it is only in the case of L//HH///X and the

236 INVEETEBKATA CHAP.

scorpion that even an approximately complete account of the life-
history has been elucidated.

If we turn to Kishinouye's account of the development of Limulus
(1893) we find that for the earliest period of development only an
incomplete series of stages was at his disposal, and that, if his con-
clusions are correct, Limulus differs from the spider inasmuch as
the nuclei which represent the endoderm are budded into the yolk
before the keel of the primitive thickening is formed. Kingsley
(1892-1893) describes the cells forming the blastoderm as dividing
tangentially into a small clear moiety which remains at the surface,
and a large inner half, full of yolk grains, which is endodermal and
wanders off into the yolk.

The primitive thickening, when it appears, is said to give rise
only to mesoderm. A similar statement, as we shall see later, has
been made for insect development, but it seems clearly to be erroneous
for insects, and may prove to be so also for Limulus. We must bear
in mind that the epithelium of the gut of Limulus is formed very
late, long after the larva is hatched, and that it appears first of
all in the region of the abdomen. Further, no coelomic sacs at all
appear in the bases of the appendages of the prosoma, except in the
fifth and sixth, and these form the coxal gland. It follows that the
coxal glands of Limulus and the spider are not strictly homologous
with one another, but that both are remnants of a once complete
series of metamerically arranged excretory organs.

As there is no anterior aorta in Limulus we find that the coelomic
sacs of the cephalic lobes do not meet each other, but that a vascular
circumoesophageal collar is formed by the shrinkage of these sacs
from the sides of the oesophagus. The heart is formed in exactly the
same way as in the spider. According to Kingsley. after giving rise
to the heart-wall the coelomic sacs fuse longitudinally with their
predecessors and successors, and so two persistent tubes are formed
which, he thinks, give rise to the genital organs, as they do in
PerijKitus (see p. 1*75).

The dorsal and ventral surfaces develop in even proportion with
one another, so that there is no process of reversion. The last
appendage of the prosoma, in the adult, has an outer branch called
the epipodite or flabellum, which is probably the remnant of an
exopodite, such as forms the major part of the limb in the case of
the appendages of the abdomen. In the embryo all the appendages
of the prosoma except the first, develop the beginnings of this exopodite,
but it only persists in the sixth and last. (Fig. 18*7, flab1'5.}

The central eyes of Limulus are inverted like the posterior
central eyes of the spider, and originate from a corresponding part
of the ectoderm ; in front of the brain rudiment on the ventral plate,
measuring along the ventral surface, behind if we measure on the
dorsal surface. The lateral eyes of Limulus originate also as a single
undivided pit on each side, as such pits begin in the spider ; but
though they develop many ommatidia, formed by the grouping of some

VIII

ARTHROPODA

237

of their cells to form retinulae, they do not become subdivided into
smaller eyes (Fig. 187, oc.l.}, each remains as an undivided compound
eye throughout life, and consists throughout of a single layer of cells ;
there is no vitelligenous layer. The lateral eyes are developed from
the sides of the cephalic lobe, and as growth proceeds the cephalic
lobe extends backwards along the sides of the prosoma, so that the
eye appears as if it belonged to the fourth segment.

The appendages of the abdomen appear as plates, each with an
inner lobe which we may regard as the endopodite ; the first pair of
appendages becomes, however, progressively reduced in size, and the

c.coe

ocl.

stom

ch

brf'

-proct

FIG. 187. — Ventral view of an embryo of Limulus longispina, 21 days old.

(After Kishinouye.)

br1, appendage bearing lirst gill book; ?«•-, appendage bearing second gill book; ch, olii'licri.-i;
chil, chilaria ; c.coe, cephalic coelom ; coe, coelomic sacs ; flab1'5, the rudiments of five pairs ni llabella,
i.e. of exopodites ; ZM5, the rudiments of the five pairs of walking legs ; l.h, lateral hump ; «•,
median eye ; m:J, lateral eye ; op, genital operculnm ; proct, proctodaeum ; stout, stomodaeum.

segment to which they belong ceases to be distinguishable. Remnants
of these appendages remain as "chilaria" forming an underlip.
The second appendage joins its fellow to form the genital operculum,
the rest form gill books.

The embryo is hatched out as the so-called " Trilobite larva "
which gradually changes into the adult. In this larva the append-
ages have all attained their adult form, but the abdomen is still
distinctly divided into segments, and each segment, seen from above,
shows a median tergum, and, on each side, a horizontally extended
pleuron, separated from it by a groove like the body segment of a
Trilobite seen from above. In the region of the prosoma we have

238

INVEKTEBKATA

CHAP.

similarly a median " glabellum," consisting of the fused terga of the
prosomatic region, and on each side of it a " fixed cheek," consisting
of the fused pleura of this region. Outside the fixed cheek there is a
marked suture or joint line, the " facial suture," which runs round
in a semicircle parallel with the edge of the carapace. The cephalic
lobe and its lateral extensions, which we may term " free cheeks," lie
beyond, and in these latter we find the compound lateral eyes (Fig. 188).
Point for point this structure is repeated in the cephalic shield of
a Trilobite, and so far the agreement between the Trilobite and the
larva is complete. But since the appendages of the Trilobite have
been made known to us by Beecher (1893) it is at once seen what a
wide divergence there is between them and those of Limulus. The

oc.

.-'•'''' 1

FIG. 188. — The Trilobite larva of Limulus. (After Kingsley.)

A, ventral view. B, dorsal view, f.c, free cheek ; f.x, facial suture ; fx.c, fixed cheek ; </?, glabellum ;
hi'ji, lobes of liver seen through ; V>, the last walking leg ; op, genital operculum.

Trilobite has unforked filiform antennae, and all the other appendages
are similar to one another. All possess a jointed endopodite with a
gnathobase, all have a rod-like exopodite which carries a " book " of
long narrow gills, essentially similar to those of Limulus, but the
contrast between the appendages of the prosoma and those of the
abdomen, which is so marked a feature in Limulus as in all true
Arachnida, is utterly absent in the Trilobite; moreover, Limulus
shows no trace of the antennae of the Trilobite.

In a word the so-called Trilobite larva represents not a Trilobite
but an Arachnid, not very unlike the adult but with segments
which are quite free from one another, and without the long tail.
Such Arachnida are known to have existed in the Silurian epoch
(ffemiaspis), but the stock from which Arachnida and Trilobita
diverged must be still further back in the remote past.

VIII

AKTHEOPODA

239

As regards the Scorpion, the embryology of which has been
worked at by many observers, the latest of whom is Brauer (1894,
1895), we find again serious modifications in the early development
as compared with that of the spider. The eggs of the scorpion are not
laid, but are retained within the body of the mother until develop-
ment has so far advanced that the young, when born, have most of
the features of the adult. The nucleus of
the ripe egg is situated not in the interior
of the egg but at its surface, and the
daughter nuclei, which result from its
division, form at first a single -layered
blastoderm extending over only a portion
of the surface of the egg. The egg is there-

germ

stom

B

FIG. 189. — Two transverse sections through the "ger-
minal disc," or developing area of the egg of the
Scorpion, Euscorpius carpathicus, in two stages.
(After Brauer. )

A, Stage of the formation of the serosa. B, stage of the
formation of the amnion. am, beginning amnion ; ect,
ectoderm ; end, endodermai nuclei; mes, mesoderm ; germ,
primitive germ cells, probably corresponding to the " primi-
tive cumulus " of the spider's egg.

FIG. 190. — Ventral view of em-
bryo of the Scorpion Evsror-
pius carpathicus showing
segments and appendages.
(After Brauer.)

a&l"?, the rudiments of the ab-
dominal appendages ; vh, rudiment
ofchelicera; cli.g, rudiment of the
cheliceran ganglion ; <-•.;//•, cephalic
groove ; c.l, caudal lobe ; I1'*, the
rudiments of the walking legs ; /«•</,

fore telolecithal and its segmentation is rudiment of pedipaip ; ^>m, open-
meroblastic, but this type of telolecithal in« of stomodaem.. ; v.g, ganglia of

" r . -11 the ventral nerve cord.

egg, as we can see by comparing it with the

egg of the spider, must have been secondarily derived from the

centrolecithal type.

At a later period cells are budded off from the blastoderm which
wander into the yolk. These cells, according to Brauer, eventually
form the endodermai epithelium, at a much later period in the develop-
ment. At the same time the edges of the blastoderm give rise to a
sheet of cells which grows backwards over it and forms a protective
cover for it, called the amnion. A little later, a second outer cover-
ing of the same kind is formed which is called the serosa (Fig. 189).

240 INVEKTEBKATA CHAP.

A keel is formed by a thickening of the blastoderm as in the spider ;
from this keel a layer of cells grows outward on each side beneath
the ectoderm, as in the spider and in Limulus, and forms the
mesoderm. Behind this primary thickening there is a second thicken-
ing formed, as Kishinouye has also described for the spider. Brauer,
however, asserts that in the scorpion this secondary thickening, or
primitive cumulus as it is called, gives rise to a group of cells which
remains unchanged for a great period of development and then gives
rise to the genital cells. There is strong presumption that this will
eventually be found to be true in the case of the spider also.

The general history of the later development of the scorpion is
very similar to that of the spider in its main outlines, but the
following points are to be noted. The egg is cylindrical and the
ventral plate only occupies one side, consequently there is no need
for reversion. But since the blastoderm only covers a portion of
the surface and is reflected at its edges to form protective membranes,
the covering of the dorsal surface of the egg with skin is effected by
the lateral growth of the ventral plate, and the pushing of its right
and left edges (that is to say, the lines of origin of serosa and amnion)
farther and farther up towards the dorsal surface, till they meet on
the mid-dorsal line, results in the protective membranes being cut
off from the egg.

Brauer could only distinguish two segments in the brain, each
marked by a transverse commissure. The lateral eyes remain as open
pits of epithelium, and they have no vitelligeuous layer. The so-called
coelomic cavity of the head or cephalic lobe is, according to him,
merely an extension of the coelomic sac belonging to the segment of
the chelicera, as may also be the case with both spider and Limulus,
in spite of Kishinouye's statement; or perhaps Brauer is mistaken
and has confused subsequent fusion with common origin.

The Malpighian tubes are outgrowths of the posterior end of the
mid-gut. Kudiments of excretory organs or so-called " nephridia "
are formed as outgrowths from the coelomic sacs in all the segments
of the prosoma from the second to the sixth, but only that one in
the fifth segment comes to full development and it forms the coxal
gland. The coelomic sacs of the abdomen press on the cells which
form the genital rudiment, and eventually these cells pass into the
interior of the first coelomic sac of this region of the body. The
genital ducts arise in exactly the same way as the " nephridia," with
which they are no doubt serially homologous.

The abdominal appendages form at first freely projecting plates,
but the first abdominal segment has only vestiges of appendages
which soon disappear and the whole segment then becomes in-
distinguishable ; the appendages of the second segment form the
genital operculum, those of the third pair form the "combs" or
pectines. The skin behind the fourth, fifth, sixth, and seventh pairs
of appendages becomes tucked in so as to form the lung sacs, and
folds on the anterior surfaces of these sacs form the lung books.

viii AETHEOPODA 241

All the nerve ganglia of the prosoma and the first pair of the
abdominal ganglion fuse to form the suboesophageal ganglion.

The heart is formed, just as in the spider, l>y the meeting of the
dorsal ends of the coelomic sacs of opposite sides. A semicircular
plate of cells is detached from the apex of each of the two coelomic
sacs, and the two grow together to enclose a blood space which is
the heart. Brauer has described in detail how the pericardium is
formed. The two semicircular plates become completely detached
from the coelomic sacs of which they once formed part, these latter
shrink away from the heart and meet beneath it, and the space
which is left between heart and conjoined coelomic sacs is the
pericardium. The coelomic sacs then lose their cavities by a process
which consists in the development of fibrils crossing their lumen,
and the swelling up and rouudiug of the cells forming their walls,
and the comparatively solid plate of connective tissue which results
forms the pericardial septum or floor of the pericardium. A similar
process then occurs in the remaining parts of the coelomic sacs, and
the only portions of their cavities which persist are found in the
coxal glands, and presumably in the genital organs, though the
origin of these latter was not traced.

What little is known of the course of development in other
orders of Arachnida fits in well with what is known of the scorpion,
spider, and Limulus. The formation of sheets of cells acting as
protective coverings to the developing embryo is not known to
occur except in the scorpion. In all cases, however, an indication
of the primitive cumulus at the hinder end of the primitive streak
can be made out, and in the Pedipalpi, according to Schimkewitsch,
the formation of mesoderm takes place from the cumulus alone.
Thus the cumulus cannot merely represent the genital rudiment
but must represent the primitive streak of Peripatus, i.e. the
obliterated section of the blastopore which occurs behind the anus
in that animal. For a similar reason the primitive streak of
Arachnida must represent the open portion of the blastopore of
Peripatus.

In the Acarina or Mites the young are hatched in an imperfect
form in which only three pairs of walking legs are developed. After
living in this state for some time they moult a thick cuticle, which,
however, remains surrounding them like a second egg-shell, called the
deutovum, inside which further development takes place and the
missing fourth pair of legs make their appearance. This reduction
of a series of homologous organs to a smaller number, in accordance
with the minute size of the embryo when hatched, is entirely in line
with what we have learnt of larval modification amongst Crustacea.

The Pentastomida, which, even when adult, are parasitic in the
nasal cavities of the dog, are supposed to be the extreme limit of
degeneration in Acarina. The larva, which encysts itself in the
connective tissue of rabbits, sheep, etc., exhibits the rudiments of
two pairs of appendages.

VOL. i it

242 INVERTEBRATA CHAP.

PANTOPODA

The Pantopoda, or sea-spiders, are treated by most zoologists as
a quite independent group of Arthropoda. Huxley, however, regarded
them as aberrant Arachnida. They agree with Arachnida in possessing
no proper jaws and in having four pairs of walking legs, but differ
from all Arachnida in the absence of the division of the body into
a prosoma with leg-like appendages in front, and an abdomen with
plate -like appendages behind, behind one of which the genital
ducts open.

In the Pantopoda the so-called abdomen is an unseginented stump
devoid of appendages, and the genital ducts, of which there may be
several pairs, open at the bases of the long legs. Further, the three
front segments bear pairs of legs reduced in size and not used for

FIG. 191. — Larva of A scorh ynclt-us mii/nfux. (After Hoek.)
chel, chelophore ; oi<, ovigerous leg; p, palpus ; stom, stomodaeal proboscis.

walking ; behind these come four pairs of walking legs, but since the
fourth of these is the seventh appendage it cannot correspond to the
last walking leg of Arachnida, though it may correspond to the
suppressed segment of Limulus and the scorpion.

The most plausible suggestion as to the origin of the Pantopoda
is that they represent a divergent branch of primitive Arachnida at
the time that these were separating from the common stock of all
Arthropoda.

The development of these interesting forms is very imperfectly
known, but what little is known only whets the desire to know
more. Thus in Pallene, according to Morgan (1891), the egg exhibits
a complete segmentation, and a blastula results, surrounded by a few
large columnar blastomeres and provided with a small blastocoele.
Later, however, just as in Brancliipus and Astacus, the inner ends of
these blastomeres coalesce to form an unseginented mass of yolk. It
appears that the endoderm is formed by budding off cells into the
yolk, and it seems likely (though Morgan denies it) that this budding

VIII

ABTHKOPODA

243

takes place in connection with a small invagination which occurs at
one pole. From the lips of this invagination at any rate the meso-
derm is developed.

It would appear that the ea-rly development of Pallene hears some
considerable resemblance to that of Palaemon (see p. 192). Pallene
emerges from the egg when it has almost attained the adult condi-
tion, but most Pantopoda emerge as larvae with three pairs of legs
and pursue a semiparasitic life inside Hydroid polyps, gradually
attaining the adult condition after a series of moults, at each of
which a new pair of legs is developed.

stem

TARDIGRADA

A word or two may here be interposed about the development of
the Tardigrada, though it is exceedingly doubtful whether these
minute, degenerate Arthropoda
are really related more closely to
Arachnida than to the other
groups. They possess no jaws or
antennae and only four pairs of
stumpy uubranched appendages.
The development of one species,
Macrobiotus macronyx, has been
worked out by Erlanger (1895).
He asserts that the minute egg
undergoes total segmentation, and
that a hollow blastula is formed
from which a gastrula arises by
invagination. From the arch-
enteron four pairs of coelomic
sacs arise as hollow outgrowths,
and there is also a median
posterior sac arising in the same
way, from which genital organs
and Malpighian tubules arise.
It is possible, however, that
Erlanger's account of the de-
velopment of the coelom is
incorrect, as it was founded on
whole mounts and not upon
sections.

oes

st

gon

FIG. 192. — Dor-sal view (optical frontal sec-
tion) of embryo of Macrobiotns i/iiir,-n, ///.,•.
(After Erlanger.)

coeJ ;{, coelomic sacs, of which the lirsf ami tin'
last can be seen to open into the gut ; yon, terminal
coelomic sac, which is the rudiment of the gnnud :
uefi, oesophagus ; s.n.ij, ectodenuic thic-keiiin.u.
rudiment of supra - oesophageal ganglion ; .-',
stomach ; xtum, rudiment of the stomodaeum.

ANCESTRAL HISTORY OF THE ARACHNIDA

When we survey the development of Arachnida so far as it is
known, we are struck by a fundamental agreement in type in animals
so diverse as Limulus, a scorpion, and a spider. In all of them the
yolk is so abundant that no trace of a complete segmentation of the

244 INVEKTEBEATA CHAP.

egg into blastomeres persists ; segmentation is represented by multi-
plication of nuclei and their arrangement at the surface of the egg.
The h'rst differentiation of layers takes place in connection with u
ventral thickening of the blastoderm, which may be regarded as
representing the blastopore of Peri-patus. The mesoderm soon
becomes split into two bands, right and left, and in each of these
a series of coelomic pockets makes their appearance.

It is difficult to decide whether Kishiuouye is right in asserting
that the first pair of these pockets is found in the cephalic lobes, and
is distinct from the pair which appears later in the segment bearing
the chelicerae, or whether Braueris right in asserting that the coelom
of the cephalic lobe is a mere forward production of the coelom of the
cheliceral segment.

If Kishinouye is right it is quite probable that the coelomic sacs
in the cephalic lobe represent a lost anterior segment in these
animals, a segment which is in front of the segment corresponding to
the first antennae of Peripatus, centipedes, and insects. As we
shall see later, this lost segment is distinctly represented and bears
vestigial appendages in the embryo of the centipede. We may
provisionally accept Kishinouye's view, remarking merely that
it seems clear that most interesting results would be obtained by a
revision of his work with the aid of modern methods, when many of
these vexed questions might be solved.

We form, therefore, the following picture to ourselves of the
manner in which Arachnida were developed. They arose from
ancestors in which all the segments except the first bore bifurcated
appendages, with plate-like exopodites and more or less leg-like
endopodites. The first pair of appendages, however, had been
modified into antennae, or tactile organs, and were subsequently lost.
The succeeding appendages had their endopodites modified into
walking and grasping organs and had lost the exopodites, whilst the
hindermost appendages retained their plate-like form and assumed
respiratory functions. Such ancestors must have closely resembled
Trilobites, but their divergence from that group consisted in this,
that in Trilobites, and to a still greater extent in Crustacea, the
appendages immediately following the antenna tended to become
gnathites (or jaws), by the diminution in size of their distal members
and the development on their proximal members of cutting blades ;
and this process went only a very small way in Arachnida, in which
the corresponding appendages functioned as the main organs of
locomotion.

.The plate-like form of limb is no doubt the original form in
Arachnida as it is in Crustacea ; and the process of transforming
these plates into rounded legs, to which the differentiation of the
front part of the body of an Arachnid is due, began in front and
travelled backwards. Pantopoda probably represent a group in which
it went farther back than in Arachnida, and in which the hiudermost
appendages were lost.

vm AKTHEOPODA 245

INSECTA

Classification adopted (only those orders specially alluded to
in the text are mentioned}—

Antera fThysanura

\Collembola

Orthoptera

Paraneuroptera (Odonata)
Hemimetabola - Ephemeroptera

[Hemiptera
( Coleoptera
I Lepidoptera

Holometabola

.Diptera

I Hymenoptera
iDii

The Insecta, even if we confine ourselves to Insecta Hexapoda
and exclude Myriapoda, are an enormous group, including nearly
three hundred thousand named species. A large amount of work has
been done on their development since the earliest days of scientific
embryology, and a full discussion of this would lead us entirely
beyond the limits assigned to this work. Fortunately, in compara-
tively recent times the embryology of two species has been worked
out in a thoroughly satisfactory manner, viz. that of Doryphora
(Leptinotarsa*) decemlineata, the so-called potato bug, or Colorado
beetle, by Wheeler (1889), and that of Donacia crassipes, by
Hirschler (1909), a beetle belonging to a closely allied family and
abundant throughout Europe. The results of these two investigators
are in agreement in all important points, but as Hirschler's work
is the most recent, we shall select Donacia and not Doryphora as
type.

DONACIA

The eggs of both forms are laid in batches enclosed in a cocoon
and attached to the under surface of leaves, those of Doryphora to
the leaves of the potato plant and allied forms, those of Donacia to
the leaves of water-plants. In studying the development of Donacia
Hirschler punctured each individual egg with a fine needle, whilst
observing the whole cocoon under a powerful dissecting microscope.
He then immersed the cocoon for two to three hours in a mixture of
equal parts of 3 per cent aqueous solution of HN03, and concentrated
aqueous solution of corrosive sublimate. The cocoons were then
passed up through grades of alcohol till they had reached that of
90 per cent, in which they remained for twenty-four hours.

Then the cocoon was cut into pieces, each of which contained
eight or ten eggs. These pieces were stained for twenty-four hours
in a half per cent watery solution of thionin, the stain being
differentiated by subsequent immersion for twenty-four hours in

246

INVEETEBEATA

CHAP.

96 per cent alcohol — a treatment which resulted in the embryonic
area being coloured dark blue, while the rest of the egg was nearly
colourless. Such eggs were then used for sections.

When it was desired to have whole mounts of the embryonic
area, the chorion was carefully removed from the individual egg by
means of a fine needle, the eggs were then stained for twenty-four
hours in borax carmine, and differentiated for the same period in
acid alcohol.

For cutting sections the fragments of the cocoon, in which all the
contained eggs were parallel to one another, with the future head ends
pointing in the same direction, were passed through xylol into paraffin.
Wheeler mentions that when he used paraffin melting at 55°, the yolky
contents of the egg took on a gummy consistency which rendered it
specially suitable for cutting, and that he got perfect sections. This
must be regarded as a somewhat exceptional circumstance, because
yolk is usually apt to become very brittle on heating, and to break up
into small fragments under the stroke of the knife, hence, usually, in
dealing with yolky eggs, preliminary embedding in celloidin, as
described in Chap. II., is desirable.

The egg of Donacia, like that of most insects, is of an elongated
oval form, and the nucleus is situated near the centre, surrounded

by an island of cytoplasm.
When the egg is fertilized
the zygote nucleus begins
to divide and gives rise to
many nuclei, each sur-
cui. rounded by its cytoplasmic
island. In Dorypliora,
Wheeler got every stage
from the first and was able
to observe that the divisions
of the daughter nuclei are
at first strictly synchronous,
so that in a given egg all
will be in the same phase
of karyokinesis. When a
been formed some of them

n

FIG. 193. — Portion of a sagittal section through the
developing egg of Doryphora (Leptinotarsa)
decemlineata before the formation of the blasto-
derm. (After Wheeler.)

cyt, peripheral layer of cytoplasm ; n, nuclei in islands
of cytoplasm ; y, yolk spheres.

considerable number of nuclei have

begin to wander outwards towards the surface of the egg whilst
others remain in the interior. This wandering seems to be due to
amoeboid movements on the part of the cytoplasmic islands which
surround the nuclei, for these are often drawn out into comet-like
shapes.

When the nuclei reach the surface they increase by further
division, and eventually form a blastoderm consisting of a layer of
columnar cells covering the whole ventral surface, and a flattened
epithelium on the dorsal surface. Towards the hinder end of the egg,
on the ventral surface, the columnar cells form a small mass several
cells deep ; this mass corresponds to the secondary thickening or

VIII

AETHEOPODA

247

primitive cumulus in an Arachnid egg, and is the first rudiment of
the genital organs. We arrive, then, at a stage when the egg is com-
pletely surrounded by a layer of cells, a blastoderm in fact, and when it
contains in its anterior a considerable number of isolated nuclei, which
become surrounded by cytoplasm and form the so-called yolk cells.

In Doryphora, according to Wheeler, the yolk subsequently
segments into a number of spherical masses, each containing two or
three nuclei and each surrounded by a thin layer of cytoplasm, and

Wheeler regards these masses as really large
yolky cells. Hirschler does not describe this
process in Donacia.

The next change which occurs is a peculiar
invagination of a portion of the dorsal blasto-
derm. At first this looks like a groove which
is overgrown from the sides by the adjacent
blastoderm, and it finally spreads out as a sheet
beneath the surface of the ectoderm. This sheet
degenerates and disappears; it is regarded as the
" primary dorsal organ," because, as we shall
see, similar processes occur at a much later stage
in development, and this later infolding struc-
ture is called the secondary dorsal organ.

germ

FIG. 194. — Surface view of
the egg of Donacia cras-
sipes at the conclusion
of blastoderm formation.
(After Hirschler.)

germ, primitive germ cells ;
ser, cells destined to form the
serosa.

FIG. 195. — Section through the dorsal part of a
developing egg of Donacia crassipes to show
the primitive dorsal organ. (After Hirschler.)

ect, blastoclermic ectoderm ; p.do, primitive dorsal
organ.

As soon as this primary infolding has taken place, the dorsal
blastoderm in front of it begins to exhibit a different character from
the blastoderm elsewhere ; its nuclei become larger and much more
widely spaced than the nuclei elsewhere (ser, Fig. 194). This peculiar
ectoderm forms a V-shaped area, with the point directed backwards
and the broad end forwards. It soon attains the anterior pole of the
egg and is the rudiment, as appears later, of the outer embryonic
membrane, the serosa. The serosa protects the embryonic area of
the egg during its development, and for this reason is termed the
sheath-ectoderm. It is probable that this peculiar change indicates
a change in physiological function ; it is suggested that the serosa
ectoderm is specially suited to promote gaseous interchange between
the egg and the surrounding medium.

248

INVERTEBEATA

CHAP.

At the same time, on the ventral side of the egg two slightly
curved longitudinal folds make their appearance, and divide the

ser

germ

jerm.

FIG. 196. — Diagrams to show the relations sustained to one another of amnion, serosa, and
embryonic area in three .successive stages of the development of Donacia crasfipes.
(After Hirschler.)

A, youngest stage. 15, intermediate stage. C, oldest stage. In eacli pair of figures the left-hand
one represents the ventral view, the right-hand one the dorsal view, am, amniotic area ; emb, em-
bryonic area ; gast.yr, the limits of the gastral groove ; germ, mass of primitive germ cells ; ser, serosa.

blastoderm into a median and two lateral plates. The median plate
gives rise to endoderm and mesoderm, whilst the lateral plates give

VIII

AETHEOPODA

249

rise to the ectoderm. A little later the area of the blastoderm with
sparse and large nuclei is seen to have spread out, so as to completely
cover the dorsal surface and also the sides of the egg, while in front
it encroaches on the ventral surface ; this change is effected, partly
at any rate, by the modification
of the cells of the blastoderm
from the previous columnar to
a flattened form.

All that is left of the
original columnar cells is a
median streak occupying the
hinder part of the ventral
surface, and reaching forward
to about a distance of one-
fourth the length of the egg
from the front end. At the
posterior end it curves over a
little on to the dorsal surface,
but between the columnar
cells of the streak and the flat
pale cells of the " sheath ecto-
derm " ordinary flat cells inter-
vene ; they form, as we shall
see directly, the amnion or
inner embryonic membrane.
The streak constitutes the
germinal disc or embryonic
area, for on it the first organs
of the embryo appear. On it
are the two curved ridges
alluded to above, which divide
it into median and lateral
plates, the last-named being
very much encroached on by
the extension of the modified
ectoderm destined to give rise
to the embryonic membrane.

Soon after this stage, at
the posterior end of the egg,
the fold appears which is
destined to cover in most of
the germinal area. This is termed the posterior amniotic fold. Its
outer limb, termed the serosa, involves almost exclusively the sheath
ectoderm ; its inner limb, termed the amnion, is composed of ordinary
blastoderm cells which pass without any break into the germinal
disc or embryonic area. A small part, however, of the embryonic area
itself is arched up into the amnion fold behind, and this is regarded
by Hirschler as a proof that the whole of the amuiotic ectoderm is

emi

germ

ser

FIG. 197.- — Diagrams to illustrate the formation
of the posterior amniotic fold in the egg of
Donacia crassipes. (After Hirschler.)

Letters as in previous figure. A, youngest stage.
B, intermediate stage. (', oldest sl.-ige.

250

INVEETEBRATA

CHAP.

A

iii reality only a secondary modification of the ordinary columnar
ectoderm.

The amniotic fold is not a simple indentation at right angles
to the germinal area ; on the contrary, it has a peculiar trilobed
growth, and the indentation is prolonged into a median and two
lateral pockets. This, however, is a feature peculiar to Donacia, and
this trilobed appearance disappears as the posterior amniotic fold
advances forward over the germinal area.

Whilst this is going on, the median field of this area becomes
markedly depressed beneath the surface, so as to form an elongated

gastral groove (qnst.gr, Fig.
198). The floor of this
groove is composed of cells
in a condition of active
proliferation, and it forms a
wedge-shaped mass in the
hinder end of the groove ;
in the middle the groove is
ser deepest and its cavity largest,

whilst in front it is very
shallow. The two sides of
the groove meet, and it
becomes thus completely
closed off from the exterior.
Throughout most of its
extent this overgrowth takes
place in such a way that
the cavity of the groove is

FICJ. 198.— Two transverse sections through the quite obliterated, but in the
gastral groove of the egg of Donacia crassipcs
after it is closed. (After Hirschler.)

ser

hinder

regon

the gastral

groove forms a hollow tube,

A, section through anterior region where the amniotic i • i i j?

folds have not yet met one another. B, section through WlllCh Can D6 S66n I0r SOine

posterior region where the amniotic fold covers the blasto- time lyilio" Under the CCtO-

derm. Letters as in previous figures. In A the gastral Jprl -,
groove is a solid cord of cells, in B it is a tube.

At the same time also

an anterior amniotic fold is formed, and grows backwards to meet
the advancing posterior amniotic fold. The two meet and fuse, the
inner or amniotic limb of one becoming continuous with the amniotic
limb of the other, and the outer limb or serosa of the one joining
the outer limb or serosa of the other.

Then the embryonic area begins to show the first signs of
segmentation. The front end has become bilobed, and these two
lobes correspond to the cephalic lobes of the crayfish. The transverse
lines which indicate the division of one segment from the next, do
not appear in regular order from before backward, but a few appear
before the others and then the rest are, so to speak, intercalated
between these. Hirschler attaches great importance to this pheno-
menon, and speaks of the embryo becoming at first divided into

VIII

AKTHEOPODA

251

"macrosegments," which subsequently are subdivided into the
definitive segments ; but as the so-called " macrosegments " do not
correspond to one another in value in different insects, it does not
appear that they have any morphological importance, or that the
appearance of the dividing lines out of their proper order is of any more
importance than the late demarcation of the chelicera segment from
the procephalic lobe in Arachnida.

In Donacia the embryonic area is first divided into a proto-
cephalic region and a so-called " protocormic " region, which includes
all the rest of the body by a single transverse line of division. The

FK;. 199. — Three surface views of the embryo of Itmiacia crassipes when the germinal stix-ak
begins to show division into segments. (After Hirschler. ;

A, ventral view of early stage. B, ventral view of later stage. C, lateral view of about the same
stage as tli at represented in B. ab, vestigial abdominal appendage; ruit, rudiment of antenna; Jiyp,
rudiments of hypopharynx ; Ji-», rudiments of tin- three walking legs ; lat>, rudiment of labrum ; mn,
rudiment of mandible ; mx1, rudiment of first maxilla ; wu2, rudiment of second maxilla ; o, mouth ; N/I'V,
rudiments of stigmatae ; stlg (at the posterior end of C), the last enlarged stigma.

protocormic region is then divided by two transverse lines into a
"jaw" region, a "thoracic" region, and an "abdominal" region.
In each of these regions the definitive segments are first marked off
at their respective hinder borders. Thus we find a stage witli two
segments in the jaw region, the hinder of which is the second
maxillary segment ; and with two in the thoracic region also, the
hinder of which is the segment of the metathorax, which later
bears the third leg. This is succeeded by a stage in winch the three
definitive jaw segments and the three thoracic segments are clearly
marked off from one another, and in which, in the abdominal region,
the last three segments are clearly delimited from one another. In

252 INYEETEBEATA CHAP.

the protocephalic region, on the contrary, the first of the three head
segments, the acron, is clearly marked off.

In the next stage the definitive segmentation is completely
attained. The head region is divided into three segments — the
acron, the antennary, and the intercalary; the jaw region into
mandibular, first maxillary, and second maxillary segments ; the
thoracic region into three segments, and the abdominal region into no
less than eleven segments. As soon as this definitive segmentation is
attained, the appendages begin to make their appearance ; first the

antennae, later the three pairs of
jaws, and then the three pairs of
legs. All these appear as broad,
slightly marked elevations, fading
out into the general level of the
segment near the mid-ventral line,
but becoming marked towards the
edges of the embryonic area.

FIG. 200.— Longitudinal section through .In fr°ut °f tne StOmodaCUm,

the abdominal appendage of the em- which has HOW appeared in the

bryo of Donacia crassipes to show its region of the first Segment, the lab-
glandular character. (After Hirschler.) -, •, T 1,1

rum appears as two broad slightly

gl, gland cells ; sec. secretum. , . -, °, . ,

marked transverse ridges, which

subsequently unite with one another. Two very small elevations
appear near the middle line behind the stomodaeum, and these sub-
sequently unite to form the apical portion of the median projection
called the hypopharynx. The latter belong to the intercalary seg-
ment, but the basal part of the hypopharynx is formed from the
sternal regions of the jaw segments. Of the abdominal segments
only the first develops an appendage, which appears as a low rounded
elevation on each side. Sections show that it is really a shallow
cup lined with columnar cells, and that it secretes a chitonous plug,
which fills up the cavity of the cup and projects on the outside.
This appendage, as development proceeds, gradually disappears, the
elevation sinking gradually to the general level of the segment again.
At a later stage the appendages have grown in length and certain
of them undergo rotation and other changes. The antennae shift
forwards so as to lie at the sides of the stomodaeum, and they are
eventually situated in front of it. The axes of the jaw segments,
instead of being at right angles to the long axis of the body, are
inclined forwards towards the mouth, and the basal portions of the
second maxillae fuse to form the labium. The labruin is composed
of an unpaired basal piece and two distal projections, and whereas it
was at first directed forwards it is now reflected backwards so as to
cover the mouth. The rudiments of the legs have grown longer and
indications of their division into joints have appeared. At the same
time, near the mid-ventral line, at the base of each appendage, a
thickening of the ectoderm is seen which is the rudiment of the
corresponding ganglion.

vm AKTHEOPODA 253

Since the appendages of the acron which constitute the labrum
are situated in the mid-ventral line between the gun gl ionic enlarge-
ments, Hirsehler is inclined to deny their homology with the other
appendages, and to suppose that they owe their origin to a secondary
division of an originally unpaired outgrowth, such as gives rise to
the labrum in lower insects.

We saw that, in an earlier stage, a gastral groove appeared in
the mid-ventral line and became closed in as a tube. Soon all trace
of a cavity in this tube disappears and the iuvaginated mass appears
as a more or less cylindrical rod, the upper end of which is wedged
into the yolk. For a while no clear boundary between it and the
ectoderm can be made out, but soon the invaginated mass is sharply
cut off from the ectoderm, first in the middle, then in the front part
of, and lastly in the hind part of the germinal streak. When this
has been accomplished the invagiuated rod flattens itself out into a
plate, remaining, however, thicker at the hinder end. Soon this plate
becomes differentiated into a median plate, which is the rudiment of
the endoderin, and two lateral plates, which are the rudiments of the
inesoderni. The median plate is only one cell in thickness, whereas
the lateral plates are each two cells thick ; both in front and behind,
however, the median plate is considerably thicker, and these regions
may be termed the anterior and posterior endodermic thickenings.

Soon the mesoderrn of the lateral plates begins to exhibit a
moniliforni structure ; in a word, it is composed of thicker pieces in
the centre of each segment and of thinner portions below the grooves
which divide the segments from one another; that is to say the rnesoderm
exhibits on each side a segmentation into somites corresponding to the
segmentation of the ectoderm, marked out by the superficial grooves
dividing the segments from one another. The mesoderm of the acron,
or procephalic segment, is, however, merely a flat plate which passes
gradually into the thickened mesoderm of the antennary segment.

Cavities now appear in many of these somites and the coelomic
sacs are thus established : they appear first in the thoracic and then
in the abdominal region, but none appear in the tenth and eleventh
segments of the abdomen. Still later a pair of sacs appear in the
segments belonging to the second maxilla, and a pair in the region
of the intercalary segment ; no other cavities appear in the head or
jaw regions. The thoracic sacs are small and round in section and
placed laterally near the points of origin of the lirnbs ; the abdominal
sacs, on the contrary, are oval in outline and extend almost to the
lateral borders of the segments.

During this time the median plate, i.e. the endoderm, has also
been undergoing differentiation. The formation of the stomodaeum
as an imagination of the embryonic area has already taken place ;
this is situated at the level of the acron and is oval in shape
with the longer axis coinciding with the long uxis of the body.
About the same time a similar invagination appears at the level of
the eleventh abdominal segment and is the rudiment of the procto-

254

INVERTEBEATA

CHAP.

emug.
covering

daeum. The stomodaeal tube projects backwards and the proctodaeal
tube forwards. As they grow in length they indent the layer
of eudoderni cells on which they impinge, and so their inner ends
become clothed, so to speak, with a layer of eudoderni cells. In the
case of the stomodaeum this layer is continuous with the anterior
endodermic thickening underneath the stomodaeum, while in its

passage backwards the stomo-
daeum passes over it. The
proctodaeal tube in its growth
forwards similarly passes over
the posterior endodermic thick -
The endodermic cells
the inner blind ends
of stomodaeum and procto-
daeuni, multiply rapidly and
give rise to two lateral streaks
of endoderm, right and left, in
front and behind, which extend
along the sides of the yolk.

Meanwhile the middle sec-
tion of the original median
band of endoderm. has broken
up into a mass of rounded cells
situated in a space which be-
comes the median section of the
epineural sinus. This, as we
have seen, is one of the first
blood spaces to be differentiated
in Peripatus, it derives its name
from the circumstance that
it lies above the rudiments of
the ganglia of the ventral nerve
cord. The newly established
lateral bands of endoderm grow
towards the middle part of the
embryo and here meet, so that
the yolk, throughout its whole
length, is covered with a layer
of endoderm cells on its lateral
surfaces. In subsequent de-
velopment these strips grow in breadth, and eventually, about the
time that the embryo hatches into a larva, the yolk is entirely sur-
rounded by a layer of endoderm cells and the mid-gut is complete.

The sub-stomodaeal endoderuial mass, which is situated under the
stomodaeum, undergoes a strange fate : it becomes divided into right
and left halves connected by a narrow bridge of endoderm, and each
half becomes divided into anterior and posterior portions which
assume the form of rounded masses adherent to the volk. Cavities

germ

6

FIG. 201. — Diagram of sagittal section (rather to
one side of median line) through the embryo
of Dunacia crassiprs to show the coelomir,
saus. (After Hirschler.)

Lc'tturs as in previous figure. In addition, un, rudi-
ment of antenna; coe.ali, coelomic sacs of the abdominal
segments ; coe.int, coelomic sac of the intercalary seg-
ment ; coe.th, coelomic sacs of the thoracic segments ; 1-
11, the abdominal segments ; gmn, primitive germ eel Is.

VIII

ARTHROPODA

255

appear in these, and when the yolk in the mid-gut is finally absorbed
a cavity appears there also. The former cavities then open into the
mid-gut cavity, and it is then seen that a secretion has been developed
in each rounded pocket, and that these pockets are in fact glandular
outgrowths of the mid-gut. Hirschler compares these outgrowths to
the liver diverticula of Arachiiida and Crustacea, they are transitory
structures and soon disappear in the larva (Fig. 203). The inner
end of the stomodaeuin is enlarged and develops a ring-like thickening
of ectoderm at its inner end ; in later stages endoderm cells become
closely pressed against this end, and individual cells wander in

amongst the ectoderm cells ;
thus when the cavity of the
stomodaeuin finally coalesces
with the mid-gut it is im-
possible to tell where ectoderm

B

mes

ends and endoderm begins.

mes

FIG. 202. —Sagittal sections through the stomodaeum
and proctotlaenm of Donacia crassipes. (After
Hirschler.)

A, through stomodaeuin. B, through proetodaeum.

n, anus ; ,-,-t, ectodermal cells ; end, endodermal cells ;
HI* -•, inesodermal cells; o, mouth.

FIG. 203. — Diagrammatic
representation of mid-gut
of the embryo of Donacia
crassipes showing its
lateral pouches. (After
Hirschler.)

ill, lateral i» niches.

We must now consider the further development of the niesoderm.
As the coelomic sacs increase in size they shrink away from the yolk
and in this way there arises a space on each side which is the lateral
portion of the epineural sinus. The two lateral spaces in the
abdominal region, where coelomic sacs of right and left sides are in
contact with one another, form from the beginning a continuous cavity;
but in the thoracic region they are converted into a single cavity
by the disintegration of the mid- ventral plate of endoderm described
above, thus giving origin to a median sinus by the joining of those
of the right and left sides.

The walls of the coelomic sac now begin to undergo differentia-
tion. The outer wall where it abuts on the ectoderm is composed of
a single layer of closely apposed cells; this is the rudiment of the

256

INVERTEBBATA

CHAP.

coe

am

B

coe

genr

body muscles. The inner wall in this region becomes converted into
a mass of cells which are somewhat loosely arranged, their nuclei lose
their chromatin, and fat drops are deposited in the bodies of the cells.
This mass is the rudiment of the glistening white fat body so char-
acteristic of insects (/.&, Fig. 208). Some cells of this fat body get
loose in the coelornic sac and tend to choke it up. Where the outer
wall of the sac passes into the inner, at its upper margin, peculiar
cells called " cardioblasts " are differentiated ; they are large cells

with clear pale nuclei, and are so
named because they take part in the
formation of the wall of the heart.

The inner wall of the coelomic
sac clings to the yolk, and as it
passes downwards it forms here a
single epithelial layer which is
destined to give rise later to the
visceral muscles. From this layer a
sheet of cells is given off which
extends underneath the yolk towards
the mid- ventral line, thus completing
the investment of the gut with
visceral muscles. Below this point
the inner wall of the coelomic sac
passes outwards to join the rudiment
of the fat body. In that part of
its course it is somewhat thickened,
and is termed, for reasons to be
explained later, the genital ridge
(Fig. 204, B). As development pro-
ceeds the coelomic sacs extend farther
and farther upwards at the sides of
the yolk, carrying the cardioblasts
on their crests.

Hirschler states that at the same
time the cavities of the coelomic
sacs open ventrally into the epineural sinus, owing to the breakdown
of the coelomic walls at this point. This statement is supported by
similar statements on the part of other authors who have worked
at the development of other species of Insecta; nevertheless it is
a statement which must be received with very great caution, because
it is at total variance with what we know of the fate of the coeloni
in other groups of the animal kingdom. For this reason we doubt
it, and think it is probable that the statement is a mistake, founded
on a result which one is apt to get by using only paraffin wax for
embedding material. When the brittle and loosely connected cells of
a yolky embryo are penetrated by hot xylol and hot melted paraffin,
diffusion currents are set up which are apt to produce artificial
ruptures, but when the tissue is slowly infiltrated by cold solution

vnc

FIG. 204. — Two transverse sections
through embryos of Donaciu crassipes
of different ages, to show the modi-
fications undergone by the coelomic
sacs. (After Hirschler.)

A, younger stage. B, older stage, amoeb,
wandering blood cells ; coe, coelomic cavity ;
ep, epineural sinus ; gen.r, genital ridge ; n.li,
neuroblast in process of division ; v.n.c,
ventral nerve cord. (In B the section passes
through a pair of ganglia.)

viii AKTHKOPODA 257

of celloidin no violent currents are set up, and the most delicate
structures are permeated and held in place. Whilst, therefore,
not denying Hirschler's statement as to the communication of the
coelomic cavities with the epiueural sinus, we are disposed to suspend
judgment on the matter till it has heen remvestigated by the aid of
more refined methods. It is to be noted that the excretory tubes of
Peripatus were confidently stated to open into the blood-spaces of
the general body-cavity, till Sedgwick, by the aid of very carefully
prepared sections, proved the contrary.

The coelomic sacs eventually reach the mid-dorsal line, and the
cardioblasts of the two sides, which have united previously with their
successors and predecessors into continuous strips of tissue, join with
one another to form the tubular heart. Throughout the greater part
of its length this union takes place at first dorsally, so that the heart
tube is for some time open to the yolk on its ventral side, but in the
hindermost region of the embryo the two lines of cardioblasts unite
at first ventrally and then dorsally, so that in this region the dorsal
wall of the heart is first formed by the ectoderm. Those portions of
the outer wall of the coelomic sacs which lie immediately beneath
the cardioblasts, unite with the corresponding pieces of the coelomic
sacs of the opposite sides to form the pericardial septum. Cells
budded partly from these strips and partly from the yolk form the
pericardial strings of cells which lie beneath the pericardium.

The anterior aorta, the only definite artery which insects possess,
is formed by the union in the raid-dorsal line of the two coelomic sacs
which belong to the intercalary segment. The aorta becomes filled
with blood cells which are derived from the loose endoderm cells at
the epineural sinus, they wander up at the sides of the yolk and get
between the two apposed rows of cardioblasts. Cardioblasts are not
found in the last two abdominal segments.

The first trace of the genital cells made its appearance coinci-
dently with the formation of the blastoderm, as a posterior thicken-
ing in that structure. When the " gastral groove " is formed this
thickening separates from the overlying blastoderm and moves
forwards, so that it is found later at the level of the tenth abdominal
segment. Then it divides into right and left halves, and the cells of
each half become to a certain extent loose from one another. This
looseness is an indication that the cells composing each heap are
actively migrating forwards, and a little later they are found pene-
trating the mesoderm in the region of the ninth segment ; still later
they are found as far forward as the seventh segment. When the
coelomic cavities have appeared the genital cells penetrate into the
"genital ridge," and in the region of the seventh segment they
increase in number and form a cylindrical mass of cells, the rudiment
of the genital organ.

The first beginnings of the central nervous system appear as two
longitudinal thickenings of ectoderm, in the stage when the embryonic
area is first definitely divided into segments. These thickenings

VOL. i s

258 INVERTEBRATA CHAP.

start at the sides of the stomodaeum; they are indeed continuous
here with thickenings in the procephalic regions which form the brain,
and they continue backwards till they join one another behind the
proctodaeum. Thus the central nervous system of Donacia, like that
of Peripatus and ofAgelena, may be regarded as a long drawn-out loop.
The ridges are separated from one another by a shallow groove, the
neural groove, which reaches from the hinder end of the stomodaeum
back to the proctodaeum.

As the appendages make their appearance the neural ridges
become segmented into thickenings lying at the bases of the append-
ages ; these form the ganglia of the ventral nerve cord. Successive
ganglia are, of course, not completely separated from one another, but
are united by thinner parts of the neural ridge, which are the
rudiments of the commissures. The inner parts of the ganglionic
rudiments soon separate from the outer larger parts, and the inner
form the definitive ganglia whilst the outermost layer forms ordinary
ectoderm. In the rudiment of the ganglion are to be seen a number
of rounded cells undergoing division. These are neuroblasts (n.b,
Fig. 204), and the cells resulting from their division are the neurons
or nerve cells.

The ectoderm lining the neural groove also becomes two layered,
and the inner layer becomes separated from the outer and forms a
peculiar median string of cells, which also enters into the formation
of the ventral nerve cord. Each lateral thickening gives rise to a
lateral group of large pale nerve cells, on the dorsal surface of which
fibrillar substance appears.

The median string of cells gives rise to three smaller groups of
ganglion cells, of which two arise from that portion of the string
which is at the level of the ganglion, and one from the inter-ganglionic
part of the median string. By the multiplication of the nerve cells,
the fibrillar substance becomes completely surrounded by them.

In Donacia no less than twenty pairs of ganglia make their
appearance, three pairs in the head, three in the jaw region, three in
the thoracic region, and eleven in the abdomen. The first three, named
appropriately protocerebrum, deuterocerebrum, and tritocerebrum,
fuse together to form the brain ; the next three unite to form the
suboesophageal ganglion, and the three last ganglia of the abdomen
unite to form a large abdominal ganglion.

Shortly after the appearance of the nerve ganglia the rudiments
of the tracheae make their appearance as ectodermal in vagi nations,
lying outside the rudiments of the ganglia and of the appendages,
when these are present. Eleven pairs of these invaginations make
their appearance on the last two segments of the thorax and on the
first nine segments of the abdomen ; they give rise to oval sacs which
unite with one another in a longitudinal direction, and result in the
great lateral tracheal stems of which the other trachea are outgrowths.
The last pair of the tracheal rudiments are larger than the rest, and
the ectoderm cells surrounding their openings (stigmata) are

VIII

AETHEOPODA

259

cylindrical and secrete abundant chitin, forming a horny ring from
which a valve-like outgrowth projects ventrally (stig, Fig. 199, 0).

We saw that as development proceeded the embryonic area
increased in length, till by the time it is fully segmented it extends
round the posterior end of the egg on to the hinder portion of the
dorsal surface. This results in what is known as the dorsal
curvature. Then the amnion and serosa become adherent to one
another in the hinder region of the embryo, and a perforation is
effected at this point. There follows a process closely analogous to
that described as reversion in the embryo of the spider ; that is to
say, the dorsal regions of the embryo grow more quickly than the
ventral, and the hinder portion of the embryo is protruded through
the hole in the membranes. The adhesion of the two membranes to
one another progresses rapidly forwards, and, step by step with
it, the tear or rip which exposes the body of the embryo increases
in extent.

The lateral portions of the embryonic area grow rapidly upwards
along the yolk towards the mid-dorsal line, and, since the embryonic
membranes arise from near the lateral edges of the embryonic area,
the lines of origin of these membranes become shifted farther and
farther upwards towards the

mid-dorsal line. When the
embryonic area has so far
extended round the sides of
the egg that its edges have
nearly met in the mid- dorsal
line, the remnants of amniou
and serosa become in-
vaginated into the yolk and
form a tube, lying along the
dorsal surface of the embryo;
this tube is termed the
secondary dorsal organ.
The formation of this dorsal
organ by the involution of
the remnants of the amnion
and serosa is progressive ; it
is begun behind and gradu-
ally travels forwards. As
soon as the invagination at
any point is complete, dis- FIG.
solution of the in vaginated
cells rapidly follows, so that

afr

205. — Two diagrammatic sagittal sections
through the egg of Periplaneta orientaMs in
two stages of development. (After Heymons.)

A, before reversion. B, after revi'sinn. nM -•"', the

at any One time the dorsal ab(lominal appendages; am, amnion; ,.d.o, secondary
Organ is Of limited extent. ,lor«il or^an ; .TO/-, serosa.

After the completion of this

organ the layer of cells of the embryonic area, which are derived from

the ectoderm, completely invests the egg. Fig. 205 shows tin; process

260

INVEETEBEATA

CHAP.

of reversion in Periplaneta, which agrees in every detail with this
process in Donacia.

About the same time the eudoderm cells have also completely
invested the yolk, and inside them the remaining yolk cells, which
from the beginning of the segmentation of the egg have remained
in the yolk, form an almost continuous layer parallel with the
endodermal epithelium and lying on it. The yolk is progressively
liquefied by the action of these cells and then absorbed. When this
is complete the yolk cells degenerate, break up, and disappear.

The excretory organs of insects are known as Malpighian tubules ;
in the adult they are long thread-like tubules which open into the
proctodaeum at its inner end. In Donacia Hirschler describes them
as arising as three pairs of short sac-like outgrowths of the procto-
daeum, in tlje stage when the embryo is still bent dorsally. When

reversion takes place these sacs
grow into long thread-like
tubes. If Hirschler's account
stiff is correct, the Malpighian tubes

*?}, J I' _ _ j_ _ J 1 • _.J_. Ti.

stu

ant

tm

£_ FIG. 206.— The "grub" of Doryphora (Leptitm-
larsa) decemlineata in the third iiistar, from
the side.

are of ectoderm al origin,
will be remembered that, in
describing the development of
the Spider, we saw in that
animal the so - called Mal-
pighian tubes arise as out-
growths of the hinder
part of the inid-gut. It
would therefore seem to fol-
low that the structures
termed Malpighian tubes in

first maxilla ; i/u:'-, second maxilla ; stiri, stigmata ;
1h. I in, thoracic imagiual discs ; «', rudiments of wings.

a.im, abdominal imaginal discs ^a»f, antenna ; m.d inSCCtS and Spidei'S are in nO

sense homologous with one
another.

The account of the embryonic development of Donacia is now
completed. Provided with digestive, circulatory, respiratory, excretory,
nervous, and muscular systems, the embryo bursts the egg-shell and
emerges as the well-known " grub," or larva of the beetle, which
immediately begins to feed on the leaves of the plant on which it
finds itself. It grows rapidly, moults several times, and then passes
into a quiescent or " pupal " stage, during which it undergoes an
extraordinary metamorphosis, and finally emerges from the pupal
skin as the perfect beetle or imago. Of the changes which convert
the grub into the beetle we have no exact account in the case of
Donacia. For the study of this process another type must be selected.

Before entering on this study, however, we shall give a very brief
survey of the most important points which have been made out in
the embryonic development of other Insecta, and we shall do this
in order to see how far they agree with the results which Hirschler
has attained in the case of Donacia.

vin ARTHROPOD A 201

OTHER INSECTA

The account which Wheeler gives of the development of the
beetle Doryphora bears out Hirschler's account of Donacia in every
important point. There are, however, several interesting features
in which Doryphora differs from Donacia. The embryonic area
extends so far on to the dorsal surface of the egg at its posterior end
that it covers two-thirds of it, consequently the embryonic area of
Doryphora encircles the egg in a longitudinal direction almost as
completely as does that of the spider. This posterior extension
occurs after amnion and serosa have been formed, and as the origin
of the posterior amniotic fold is forced farther and farther forward
on to the dorsal surface of the egg, by the growth in length of the
embryonic area, yolk passes in between its two limbs, i.e. between the
amnion and serosa.

The serosa ultimately forms a complete envelope, its anterior and
posterior folds meeting one another as they do in the Vertebrate
embryo. It then separates from the egg completely and adheres
to the egg-shell, consequently, when reversion begins, only the
amniou is ruptured and only the remnant of the amnion forms the
secondary dorsal organ. The grub of Doryphora has three pairs of
larval eyes (and this is true of Donacia also) ; they arise as little
ectodermal pits on the side of the head, in each of which the central
cell is larger and clearer than the others.

But Wheeler (1889) has also studied the development of Blatta, a
cockroach and member of the order Orthoptera, a group of insects
which differ from the Coleoptera inasmuch as they emerge from
the egg as perfect insects except for the want of wings.

In the case of Blatta the embryonic area is always confined to
the ventral surface of the egg and is never as long as the egg. The
mode of formation of the primary layers differs from the mode
observed in Doryphora and Donacia in several important points.
There is no gastral groove, but a posterior blastoporal pit, the cells
lining which proliferate actively, giving rise to two streaks of
cells which extend forwards and constitute the lateral bands of
mesoderm. When the coeloniic sacs make their appearance those
in the thorax extend into the legs as in Peripatus, and are not
confined to the bases of the leg as in Donacia. No trace of the
endoderm can be distinguished until a much later period. When
it is seen it consists of two thin bands of very small cells lying
on the lateral surface of the yolk and connected with sheets of
similar cells attached to the inner ends of stomodaeum and
proctodaeum.

By this time, however, the mesoderm has become segmented and
has developed coelomic cavities, and the walls of these have under-
gone differentiation.

From the similarity of the endoderm in Blatta at this stage to its
condition at an earlier stage in Doryphora, Wheeler concludes that

262 INVEETEBEATA CHAP.

in Blatta also the endoderm has been derived from the cells of those
bands to which the blastoporal pit gives rise.

Heymons (1894) has, however, drawn a completely contrary con-
clusion from his study of Orthoptera. According to him the thin
sheets of cells attached to the stomodaeum and proctodaeum (end,
Fig. 202, A and B) have arisen by the proliferation of the inner ends
of those structures, and are therefore ectodermal in character ; he
thus draws the conclusion that the " eudoderrnal bands " must,
therefore, also have an ectodermal origin, and that for the same
reason the epithelium lining the whole of the alimentary canal of
the higher insects must be ectodermal in character. Finally, he
supposed that the true eudoderm, which must have existed in the
ancestral insect, was represented in most modern Orthoptera by
degenerated yolk cells.

Heymons and his pupils have sought to show that this conclusion
is true for all the higher Insecta, including the Coleoptera, though
they admit that in the lower Insecta a true endoderm is present.

It is the merit of Hirschler to have shown the untenability of
this theory, which is at complete variance with what is known from
the study of all divisions of the animal kingdom. Wherever experi-
ment can be applied (see p. 525), it is always found that ectoderm and
endoderm are physiologically differentiated, that they possess different
organ-forming substances which make them functionally irreversible.

Heymons' error is a good example of the kind of trap into which
embryologists may fall ; lie has chosen a case on which to base this
theory where the endodermal rudiment becomes distinguishable only
at a very late stage of development, and where its first origin is
impossible to determine with accuracy. It is almost certain that
he never would have propounded such a theory if he had begun with
cases where the differentiation of the layers is a more simultaneous
proceeding. The whole of Heymons' theory stands or falls with the
assumption that the sheets of cells attached to the inner ends of
stomodaeum and proctodaeum are derived from those structures, and
of this he gives no proof.

The embryo of Blatta develops large compound eyes on the
cephalic lobes before leaving the egg, but their development has not
been minutely studied. Blatta likewise differs widely from Dory-
phora inasmuch as the embryo develops rudiments of appendages
on all the segments of the abdomen (al, Fig. 205) ; of these, the
appendages of the first abdominal segment have a glandular structure
as in Doryphora, the last pair of the appendages persist as the anal
cerci and all the rest disappear.

The development of the genital organs in Phyllodromia, another
genus of Orthoptera closely allied to Blatta, has been worked out in
great detail by Heymons (1891). The original genital cells, which
we may term primitive germ cells, and which doubtless originate
at the hinder end of the embryonic area, as in Donacia, were first
recognized as large cells with pale nuclei lying between the yolk

VIII

ARTHROrODA

263

and the unsegmented mesoderm in the abdominal region. When
the division of the embryonic area into segments takes place, they
are found in segments 2-7 of the abdomen, in the coelomic wall in
the region of the genital ridge, as in Donacia. To them are added
modified coelomic cells, which we may term secondary germ cells, and,
together with the primary germ cells, they form a continuous mass
on each- side, which is the rudiment of the genital organ ; they are at
first found between contiguous coelomic sacs as well as in their walls.
When the coelomic sacs become choked up by the development of the
fat body, the uppermost section of each retains a slit-like lumen, the
inner wall of which is formed partly by the genital mass, the outer by
the layer of cells which gives rise to the pericardial septum. Above
the genital mass the inner wall is formed by a thin sheet of cells, the
so-called filament plate (fil.p, Figs. 208 and 209). Later^the slit-like

FICJ. 207. — Longitudinal section through the embryonic area of an embryo of
Phyllodromia germanica. (After Heynions.)

coe, coelomic sac ; j/1, germ cell produced before the coelom is dislodged ; g2, germ cell
formed from the wall of the coelomic sac.

lumen disappears entirely, and this sheet breaks up into eight
vertical threads, united above by a longitudinal thread ; these are
the terminal threads of the ovarian tubes. Soon the genital mass
also becomes divided into vertical strings connected by a longitudinal
piece below. The eight vertical strings form the eight ovarian tubes
and the piece connecting them gives rise to the common oviduct on
each side. In the larval stage there are two oviducts. When the
adult condition is attained, a median oviduct is formed as an ectodermal
invagination, and into this the two oviducts of the larval period open.

When we survey the rest of the Insect world, we hud that the
most interesting divergences from the types we have just studied are
presented by the Apterous insects whose development has been
studied by Heymons (1897 and 1905). By common consent these
insects are placed at the bottom of the class to which they belong.

The development of Lepisma shows that the early stages of
segmentation, etc., resemble those of Donacia; there is the same
multiplication of nuclei and the same migration of these nuclei to

264

INVEETEBEATA

CHAP.

the surface. We find also an embryonic area from which nuclei are
budded off into the interior, but this area is very short indeed

coe

coe

v.m-

v.nc.

Fi«. 208. — Transverse sections through three einliryos of Phyllodromia gennanica at three
stages of development in order to show the development of the coelomic sacs. The
fat liody, and the generative organs. (After Heymons.)

A, the youngest stage. B, intermediate stage. C, oldest stage, after the completion of the dorsal
surface, coe, coelomic sac ; up, epineural sinus ; f.li, fat body ; fil.p, terminal filament plate of the genital
organ ; </, germ cells ; gen, accumulation of germ colls forming the genital organ ; H, heart ; stig, stigma
of trachea ; v.m, ventral longitudinal nerve ; v.n.c, ventral nerve cord.

compared to the length of the egg. The cells which are budded
inwards give rise to the yolk cells, and also to those cells which, at a

fll

p • • * ^ ~'

•Ty;>7-' ,.••'•' 0 '* ' •-'•is .-:7-\

Fie. 209. — The rudiment of the female genital organs of /'/ii/f/in/nniiifi
reconstructed from sagittal sections. (After Heymons.)

Jil, terminal lilament ; ,fil.]i, plate uniting u]>per ends nf tin- terminal filaments ; germ, germ cells ;

iir/l, rudiment nt oviduct.

comparatively late period in development, assemble on the surface
of the yolk and constitute the endoderm.

The mesodermic bands arise later by proliferation from the

VIII

ARTHEOPODA

265

embryonic area, and then segmentation of the embryonic area occurs ;
there is, however, no gastral groove. An intercalary segment is
clearly indicated. All the abdominal segments develop appendages.
Of the three anal cerci which the adult possesses, the two lateral
represent the appendages of the eleventh abdominal segment, the
median a backward prolongation of the telson. The genital cells, as in
Donaeia, originate from a group situated in the posterior end of the
embryonic area ; they wander forward and are eventually found in
the dorsal section of the somites.

The most interesting feature in the development of Lcpisma
concerns the formation of membranes. As the embryonic area
becomes segmented it becomes bodily invaginated into the yolk, but
the opening of the invagination, which we may term the amniotic
pore, is never closed. It follows that the greater part] of the

am

am.p

emb

FIG. 210. — Two views of the egg Lcpisma saccharina in different stages of development.

(After Heymons.)

A, sagittal section of the stage of invagination of the embryonic area. B, external view, stage of
exsertion of embryo. a»i, amnion ; am.p, amniotic pore; cmb, embryonic area; ser, serosa ; s.il.n,
secondary dorsal organ ; y, yolk.

ectoderm covering the egg corresponds to the serosa, and the nuclei
of these ectodermal cells undergo the same characteristic modifica-
tion as do the nuclei of the serosa cells of Donaeia. The lateral
walls of the invagination cavity, as they pass down to join the ends
of the embryonic area, consist of ordinary flat cells with normal
nuclei and correspond to the amnion.

Turning to another representative of the Aptera, Ma-chilis, which
is unique amongst insects in retaining rudimentary appendages on
the abdomen throughout life, we find still more primitive conditions.
Here, too, the embryonic area becomes invaginated, but the iu-
vagination is not deep, and a comparatively large opening connects
the invagination cavity with the exterior. The front half of the egg
alone is covered with ectoderm, whose nuclei undergo the characteristic
serosa modification; the hinder half remains covered with cells having
ordinary nuclei, and represents the amnion. Heymons suggests
that the serosa ectoderm, with its peculiar nuclei, has a distinct
physiological function, possibly connected with the transfusion of gas.

266

INVERTEBRATA

CHAP.

ser

The remarkable agreement in all essential details between the
development of a primitive insect like Lepisma and a highly modified
one like Donacia, which is disclosed by Heymons' researches, enables
one to pass over the embryonic development of other groups quickly.
In Odonata (Paraneuroptera) the embryonic area is comparatively
short, and the hinder end is invaginated into the interior of the egg ;

or to put it in another way,
there is only a posterior, no
anterior amniotic fold ; but
in all the higher insects, as
in Donacia, there are both
anterior and posterior am-
niotic folds, and this is the
case in true Orthoptera.

In the Lepidoptera yolk
spheres pass in between
amnion and serosa after the
front and back amnion folds
have united, so that the
embryonic area is said to be
immersed. In Lepidoptera,
too, all the abdominal seg-
ments develop appendages,
and these are retained on
those segments which, in
the caterpillar larva, possess
sucker feet.

In those Hymenoptera
which possess a caterpillar-
like larva, the same thing is

FIG. 211.— Two diagrammatic lateral views through true. It IS true also of

the egg of Machilis alternata in different stages many Coleopterous embryos,

of development. (After Heymons.) ^ Melolontha. In these

A stage of incipient imagination of the embryo. larvae_in early stageS— all

B, stage of more complete mvagination of the embryo. J

Letters as in previous figure. the abdominal segments

have appendages, but all

disappear except that on the first abdominal segment, which lasts a
long time and becomes glandular.

The eggs of Diptera, which develop very rapidly, show a
comparatively long embryonic area, and the same is true of the
rapidly developing parthenogeuetic eggs of Hemiptera. In fact, the
variation in relative size of embryonic area and yolk seems to be
the most important feature in the eggs of different kinds of insects.

ser

METAMORPHOSIS

We shall now consider the second stage of the development of
insects, viz. the metamorphosis of the larva into the adult form. The

VIII

ARTHEOPODA

267

most recent and elaborate work on this subject has been done by
Poyarkoff (1910). He studied the metamorphosis of a beetle,
Galerucella ulmi, belonging to the family Chrysomelidae, i.e. to the
family to which Donacia and Doryphora also belong. Poyarkoff used
picroformol dissolved in alcohol at 60° C. to preserve the larvae,
cutting them open so as to allow the fluid to penetrate.

The~ larva possesses nine visible abdominal segments, from which,
however, all trace of appendages has vanished. The thorax bears three
pairs of legs, each consisting of a based
piece and of a single joint. The head
carries mandibles, two pairs of maxillae,
and a single pair of rudimentary ocelli.
The antennae are only represented by
knobs. The stomodaeum swells out into
a pharynx which is longitudinally ridged ;
behind this is a valve -like fold which
marks the beginning of the long mid-gut.
The mid -gut runs back to nearly the
posterior end of the body, then turns
forward till it reaches the front end of the
abdomen, and then turns backward again, mg
When it has reached as far back as the
end of the first limb there is a constriction
which separates it from the proctodaeum.
The proctodaeum consists of a portion
partly invaginated in a valve-like manner
into the mid -gut, followed by a second
section with six longitudinal folds which
is produced into a caecal pocket : this
section turns forwards. A third section
bends backwards again and is suddenly
constricted to form a fourth section, which
is the true rectum. From the caecal pocket
the four enormously long Malpighian
tubules arise ; they run nearly to the front
end of the body, then bend back and have
their terminal sections closely applied to
the third section of the proctodaeum. A

map

prod

212- "

a

of the

anatomy of the larva of
Gali'i'ui'i'll/i ulmi. (After
Poyarkoff. )

a, anus ; w</', «;/-, »*;/•', the first,
second, and third limbs of tin1 niiil-
gut ; mat*, Malpighian tubules; u,
mouth ; /nvct, proctodaeum ; W,
pair of Salivary glands opens into the salivary gland ; sfom, stomodaeum.

buccal cavity.

There are eight pairs of stigmata in the abdomen, one pair on the
mesothorax and a rudimentary pair on the metathorax. There is a
" brain " and twelve pair of ventral ganglia — the first being the
suboesophageal ganglia. There is, of course, a dorsal tubular heart
in the abdominal region. Bound the bases of the antennae and of
the legs there are imaginal discs which are slightly folded portions
of the ectoderm ; the cells forming these discs remain in an embryonic
condition aud do not secrete cuticle. On the dorsal surfaces of the

268 INVEETEBEATA CHAP.

second and third segments of the thorax there are pairs of similar
imaginal discs which later become infolded, and from the bottoms
of these discs, in the later larval life, small buds grow up which are
the rudiments of the wings.

The larva when hatched is 1 mm. long ; it moults about
seven times and grows rapidly after each moult, so that when ready
to metamorphose it is 8-10 mm. long. It then stops eating, since the
epithelium of the mid-gut has already been cast off, and it moves more
and more slowly, for the muscles moving its limbs are beginning
to undergo destruction. Then it becomes bent double ; it remains
so for a period of twenty-four hours, and during that time the
muscles of the legs are completely destroyed, and the salivary glands
share the same fate. Finally, the cuticle is moulted and the larva
becomes a pupa, which in external form and proportions resembles
the adult beetle ; the antennae and the legs have reached the
definite proportions attained in the adult, but the wings are short
and motionless. Eight or nine days afterwards a second moult
occurs, and the perfect insect, or imago, emerges.

The principal part of Poyarkoff "s investigations concern the histol-
ogical changes which occur during the metamorphosis. He established
the fact that, broadly speaking, the larval ectoderm becomes the adult
ectoderm, but that the nucleus of each cell expels part of its
chroma tin, which passes to the base of the cell, surrounds itself with
a ball of cytoplasm, and is then cut off from the rest of the cell.
This ball lies between the bases of neighbouring ectoderm cells, and
while in this position is devoured by amoebocytes.

In the case of the " tendon " ectoderm cells, in which a portion of
the cell is transformed into fibres to which larval muscles are
attached, this tendinous part is thrown off from the rest of the cell
and is then devoured by amoebocytes like the balls derived from the
other ectoderm cells. In some ectoderm cells, however, the nucleus
is absorbed in situ, and then the whole cell degenerates and is eaten
by amoebocytes. Many of the ectoderm cells are glandular ; they
have narrow necks and enlarged basal portions with three nuclei, and
they persist in the pupa.

When the larval cuticle is thrown off the basal part of the
pedicel of the gland cell grows and forms a connection with the cuticle
of the pupa. There are a series of gland cells situated in the neck fold
of the larva, between the head and the first segment of the thorax,
each of which has several ducts ; these round themselves off into
balls, drop off, and are devoured by amoebocytes. Even those glands
which, as we have seen, persist into the pupa stage, undergo destruc-
tion in a similar fashion when the pupa moults in order to become
an imago. The glands of the adult are developed out of ordinary
ectoderm cells.

The changes which occur in the alimentary canal are as follows.
The first thing to be noticed at the onset of metamorphoses is an
increase of the cells on both sides of the valve separating stomodaeum

VIII

AETHEOPODA

269

and intestine. The cells on the stomodaeal side elongate so as to
block the cavity of the oesophagus : they cast out refractive granules,
and then, at the final moult, flatten out and form the lining of the
adult oesophagus. The cells on the mid-gut side of the valve multiply
very rapidly and form a plug completely obliterating the lumen of the
mid-gut. The old mid-gut epithelium is stripped off from its base-
ment membrane and is devoured by amoebocytes penetrating from the
body-cavity. The whole mid-gut is shortened till it is about one
fourth of its former length, but Poyarkoff could not determine how
this comes about. Then a new provisional epithelium is reconstituted

stem

B

FIG. 213. — Portions of sections through the valve separating stomoilaeum from mid-gut
iu the larva of <iah-ni<-cUn_ xl/iti. (After Poyarkolf. )

A, in the well-developed larva. B. in the larva on the point of metamorphosis, rut, cuticle lining
the stomodaeum ; l.i-iid, larval endoderm ; ii.eml, pupal endoderm ; stom, stomodaeuni ; v, valve.

from some of the cells forming the plug. This epithelium lasts
during the pupal stage, at the close of which it is thrown off and
the definitive epithelium of the mid-gut is formed from other cells
of the plug which have hitherto remained undifferentiated.

The epithelium lining the hind-gut or proctodaeum behaves very
much like that lining the stomodaeum ; the cells cast out granules
and then flatten, in other words the basal part of each cell rejuvenates
itself. Then the folds in the proctodaeum flatten out and the cells
become cylindrical ; this shape they retain in the pupal stage, but
when the adult stage is reached these cells flatten out again. The
salivary glands of the larva are entirely destroyed by amoebocytes,
but new salivary glands are formed in the pupa when it is three days

270

INVEETEBEATA

CHAP.

old, appearing as a pair of ectodermic invaginations at the bases of
the first maxillae.

The Malpighian tubes undergo curious changes. They are lined
in the larva with large granular cells, and at intervals between these
cells small replacement cells are seen. When the metamorphosis
begins these small replacement cells multiply, become fusiform, and
pass inwards till they form a string occupying the axis of the tube.
The string becomes hollowed out and forms the lining of the adult
Malpighian tube, whilst the cells which formed the lining in the
larva gradually liquefy (Fig. 215) and their remains are removed by
amoebocytes.

FIG. 214. — Sections of the epithelium of the
mid-gut in the pupa of Galerucella itlmi
showing the changes undergone by the
metamorphosis into the adult condition.
(After Poyarkoff.)

A, from the gut of a pupa four days old. B,
from the gut of a pupa five days old. C, from the

FIG. 215. — Portions of the Malpighian
tubes of a larva and a pupa of Galeru-
cclla ulmi. (After Poyarkoff.)

A, tube of larva. B, tube of larva just

gut of a pupa seven days old. a. end, adult endo- beginning to pupate. I. it, larval nuclei; J>.H,

(lnrm ; ji.i.:mJ, pupal endoderm.

pupal nuclei.

Finally, many of the muscles of the larva disappear; first the
striation is lost and the cytoplasm forms a homogeneous mass, then
the nuclei multiply and become dispersed through it, and then the
whole mass is attacked and devoured by amoebocytes. The corre-
sponding adult muscles are formed by the growth and elongation of
masses of small oval mesodermic cells which are attached to the
inner sides of the corresponding "imagiual discs" (Fig. 216). In the
case of some larval muscles, however, such as the powerful adductor
mandibuli, a portion of the cytoplasm persists and is not eaten by
amoebocytes, and its nuclei multiply and it becomes converted into
the fibres of the adult muscle. The changes in the heart and in
the nervous system were not examined by Poyarkoff.

Poyarkoff did not study the development of the wings in

VIII

ARTHROPODA

271

Galerucella, but it has been carefully worked out iu Doryphora by
Tower (1909). The first traces of the wings appear before the
embryo is hatched as small oval piguiented areas situated on the
sides of the mesothorax and metathorax, just below the spot where,
later, the tergum ends aud the pleuron begins. They are therefore
about the same level as the

stigmata which are situated

the

imoeb

1C

FIG. 216. — Portion of the abdominal muscles of
the larva of (Jalentcelln. itfini undergoing
histolysis. (After Poyarkotf. )

on the segments of
abdomen. When the areas
thus marked out are ex-
amined by sections they are
found to consist of elongated
columnar ectoderm cells-
distinguished from the other
ectoderm cells merely by
their depth and their slender
character, so that they appear i'
crowded together. In each
area a circular pit appears
which lengthens to form a
longitudinal furrow. This
furrow deepens till the whole
imaginal disc consists of a
longitudinal fold of ectoderm
with merely a virtual cavity.
The dorsal limb of this fold

1 ,i • -i ,i ,1 iini'ii'h, amoebocytes which ingest the larval muscles;

Clie i.c, imaginal cells, which build up adult muscle; Z.miwc,
Ventral, and from this dorsal larval muscle fibres ; l.n, larval nuclei.

limb, during larval life, the

actual wing rudiment grows out as a protuberant fold of ectoderm.
The thinner ventral limb of the imagiual fold, which forms what
we may term the wing sac, is passively stretched during the process ;
but not until the moult takes place which transforms the larva into
a pupa do the limbs of the original fold come apart and allow the
wing to protrude as an external appendage.

The wing consists at first merely of two layers of pillar-shaped
ectoderm cells each underlaid by a thin layer of mesoderm, such as
everywhere underlies the ectoderm, forming a kind of dermis. The
layer of mesoderm secretes a strong basement membrane on which
the inner ends of these cells rest. The two basement membranes,
corresponding to the two sides of the wing fold, are mostly in contact
with one another, but in certain places they remain separated, leaving
in this way spaces, bounded on both sides by basement membrane,
some of which are in open communication with the general body-
cavity.

These spaces are the primary veins of the wing ; they become
much swollen during the pupal moult, for the abdomen contracts
and its contained blood is necessarily forced forwards. At the same

w ws

FIG. 217. — Diagrammatic sections through the imaginal disc of a wing in various stages of
development, showing how the wings develop in various groups of insects. (After Tower.)

A, wing'development in Orthoptera, Odonata (Paraneuroptera), Ephemeroptera, and many families
of Colooptera (cf. Cerambycidae and Buprestidae). B, wing development in Lepidoptera and in
Chrysomelidae (including the genera I>niiiii-!n, /'nn^'/iom, and Galerucclla amongst Coleoptera). C, wing
development amongst the higher Diptera (Muscidae). nd, cuticle; if, trachea; ic, rudiment of wing ;
w.s, wing-.s;ic.

272

VIII

AETHEOPODA

27;-;

time the nuclei and cytoplasm of the ectodermal cells of the wing
migrate outwards, and the basal portions of these cells contract till
they form attenuated fibres attached to the basement membrane ;
in this way wide spaces are formed between neighbouring ectoderm
cells.

In the wing rudiment of the larva there are two tracheae arising
from the dorsal longitudinal trunk, which grow in along the course
of the wing veins. Towards the end of the larval period these
tracheae give off abundant branches, the tracheoles, which penetrate
into the spaces between the bases of the ectoderm cells, and in each
of these cellular outgrowths a delicate coiled tube develops. During
the pupal stage these tracheoles
seem to be absorbed by the blood,
but new tracheoles are developed
in the adult wing as evaginations

ant

FIG. 218. — Two views of the head of the larva of 7>////.xr^.v muryi nulls, in two stages
of development. (After Giinther. )

A, in aquatic larva. B, in larva about to pupate, nut, antenna ; es, eye-spot of the larva ; rU1, 1ms > ,f
eye-spot carried away by loosening cuticle ; mn, inaudible; m.c1, first maxilla ; (M2, second maxilla;
oc.c, rudiment of compound eye ; oc.s, simple eyes ; ocis1, lenses of the simple eyes carried a\v,i\
from them by the loosening of the cuticle.

from the tracheae. Besides tracheoles, blood and leucocytes are
the only other elements which enter the wings. The muscles

moving; them are confined to their bases and are attached to the

O

thorax.

The development of the larval and adult eyes has been most fully
worked out by Giinther (1912) in the case of Dytiscus m«r<ji null*, a
beetle belonging to the family of water-beetles (Dytiscidae). The larva
has six ocelli on each side of the head, and in addition a rudimentary
eye-spot. The ocelli are arranged in a vertical ellipse, and when
examined by sections each is found to constitute a slit-like pit.
The cells constituting the base of the pit carry visual rods ; each
rod consists of two semicyliudrical pieces adherent to each other,
and each piece seems to consist of a mass of agglutinated delicate
fibrillae. The cells lining the sides bear horizontally directed

VOL. I T

274

INVERTEBRATA

CHAP.

lens

yit

visual rods, much smaller than the basal rods but of the same
character. Above these horizontal visual cells come cells bearing

pigment, which form the upper part
of the wall of the pit. At the
edges of the pit are cells which
secrete a "glass body," that is a
mass of gelatinous refracting sub-
stance, whilst outside these again are
the cells which secrete the thicken-
ing of the ordinary cuticle termed
the lens (Fig. 219).

When the larva leaves the water
and seeks a spot on land to bury
itself and undergo the pupal moult,
a fine pigmented line can be observed
surrounding each group of ocelli
like a horse-shoe. As development
proceeds, this horseshoe-shaped line
thickens, aud the lenses of the ocelli
are torn away from the deeper
pigmeuted portions, since the lenses
belong to the larval cuticle which
is now being stripped off. The
horse-shoe pigmented area has now
increased in breadth till it has
become a broad crescent, and the
pigmented portions of the ocelli are
close to its concave border.

Soon, before the final moult to
form the

FIG. 219. — Longitudinal section through
simple eye of larva of Dytiscus mar-
fllitnlin parallel to its shortest
diameter. (After Giinther. )

ect, ordinary ectoderm : n.f, nerve fibres;
l.v.c, large visual cells; l.r.r, large visual
rods; s.v.c, small visual cells; s.v.r, small
visual rods ; vit, vitelligenous substance.

imago

is completed, the

oc.s

FIG. 220. — Lateral views of the head of the larva, of Dytiscus maryintilis, in three stages
of development, to show the gradual growth of the rudiment of the compound eye.
(After Giinther.)

Letters as in Fig. 218. net, line of setan, marking posterior limit of eye area.

remnants of the ocelli recede from the surface altogether, and the
pigmented area now becomes also circular in outline, and spreads over

VIII

ARTHROPODA

275

the place the ocelli originally occupied. The remnants of the ocelli
remain during life as closed pigmented vesicles attached to the
optic nerves. The horseshoe-shaped pigmented area is, of course,
the " imaginal disc " of the adult compound eye. The ectoderm here

b.c.

FIG. 221. — Two stages in the development of the compound eye of l>ytiscns
as seen in longitudinal section. (After Giinther. )

A, in the stage of lirst differentiation of the n-t.inul.-u>. B, in the stage of crystalline conr-fm IIKI-
tion. li.r, basal cell; l.c, cells which form the lens; pig, pigment-secreting cell; rli, rhabdome
)'. rudiment of retinula ; vit.c, crystalline cone cell.

hecornes thick and consists of narrow columnar cells, whose nuclei are
disposed at several levels though they still constitute a single layer
of cells.

At one end of the horse-shoe there is a spot where the cell limits
cannot be distinguished, and the ectoderm appears to consist of a

!76

INVEETEBEATA

CHAP.

thick mass with numerous nuclei scattered through it ; this is the
area of proliferation from which, for a considerable time, new com-
ponents (ommatidia) are added to the compound eye. Throughout
the rest of the area, certain groups of cells now become entirely
retracted from the outer surface and their protoplasm becomes
clearer; these are the rudiments of the retinulae. Each group
consists of eight cells, one central and seven peripheral ; one of these

peripheral cells is squeezed out from between
the rest, while the central cell and the remaining
six peripheral cells co-operate in forming one
long visual rod or rhabdome ; the lower end of
this rod originates as a thick piece in the basal
cell whilst its upper part tails out to a fine
point before reaching the upper limit of the
retinula cells (Fig. 221).

Above each retinula, and intervening between
it and the ectoderm, are specially modified
ectoderm cells which are comparatively short,
and whose bodies are filled with clear vesicles.
Cross-sections show that a group of four such
cells is situated above each retinula. The clear
vesicles in each cell amalgamate to form a clear
rod, and the four clear rods belonging to the
four cells cohere to form the crystalline cone.
The cone cells and the retinula together constitute
an ommatidium. The cells between adjacent
ommatidia extend through the entire thickness
of the ectoderm and secrete pigment. The upper
ends of these cells secrete the cuticle that covers
the whole rudiment, but above the crystalline
cone cells, where they bend to meet each other,
they form a thicker area of cuticle known as
the lens. In both ocelli and adult eye the
FIG. 222.— A small por- nerve fibres of the optic nerve are basal out-
tion of the adult com- growths of the retinal cells.

pound eye of Dyti*-,,* It is obvious on considering the facts which

marginalis, as seen in . ... . ,

longitudinal section, have just been related that both ocelli and the

ommatidia of the adult eyes are to be looked on
as ectoderrnal pits. The ommatidium is, however,
much simplified and specialized as compared with
the ocellus : it possesses one large visual rod,
not many small ones, and its " glass body " is formed not of an
amorphous mass of secretion but of four definitely shaped fragments
which cohere. The bearing of these facts will be considered when
we come to treat of the phylogeuy of Insecta.

For his work on the eye Giiuther used as preserving mixture
Flemming's fluid, and also a mixture of 3 parts absolute alcohol, and
1 part glacial acetic acid. After the material was embedded the

(After Giinther.)

Letters as in previous
figure; /, Ions; rit, crystal-
line cone.

VIII

APtTHROPODA

277

hard external cuticle was pared off by a fine scalpel, and the spot
so exposed was covered with fresh paraffin.

The metamorphosis of the family Chrysomelidae, amongst
Coleoptera, which we have studied in ti<ilcni.cella and Dorypliora, is
very simple as compared to the metamorphosis of the family Muscidae
in Diptera. The latter may be regarded as exhibiting the most
complicated metamorphic process of all Insecta. Amongst the
Coleoptera, however, which have a more prolonged period of larval
existence than the Chrysomelidae, still simpler conditions are found,

Fie. 223. — Diagrams illustrating the metamorphosis of Musca rontitoria. (After Van Rees. )

A, maggot with deeply embedded imaginal discs. B, early stage of pupation. C, later stap> <>!'
pupation. abl, Hrst abdominal segment; re/i/t, head region largely invaginated, the inva.uinatrd part
represented by a white lino ; rut, cast-oft' cuticle ; /'•'', the imaginal discs for tin- legs, each enclosed
in its sac; halt, imaginal disc for halteres ("balancers"); M''::, the three thoracic segments; w,
imaginal disc for wing.

so that little difference is to be detected between their life-histories
and those of the so-called Hemimetabolous insects, such as Orthoptera,
Odonata (1'araneuroptera), and Hemiptera. Thus, according to Tower,
in many Coleoptera, and in particular in the families Cerambycidae and
Buprestidae, the imaginal disc for the wing consists of an area of
ectoderm which shrinks away from the larval cuticle, dipping very
slightly below the general level. On this area the wing develops as
an external appendage. The imaginal discs only apprar towards the
close of larval life (Fig. 217, A).

A slightly more complicated condition is found in the family
Scarabaeidae where the imaginal disc, which likewise appears lair,

278

INVEETEBEATA

CHAP.

forms a deep pouch with wide opening from the bottom, out of which
the wing grows up. This condition is found in the more primitive
Diptera, such as Culicidae and Tipulidae, which also have long
antennae. The Lepidoptera agree with the Chrysonielidae in their
mode of wing development. It is obvious that the only difference
between the development of a Buprestid beetle and an Orthopteran is
that the Orthopteran is active at all stages of larval life till the adult
condition is attained, whereas in the Buprestid a quiescent stage, the
pupal condition, intervenes between larval and adult stages.

On the other hand, the development of Muscidae among Diptera,
a group to which our house- and blue-bottle flies belong, shows, as
lias been already mentioned, very complicated conditions, which have

cul

OC.C

v.n.c.

FIG. 224. — Two diagrams illustrating the metamorphosis of the head of Mi/sen vomitoria.

(After Van Eees. )

A, early pupa, in which the head region is still invaginated. B, later pupa, in which the head
region is evaginated. (Hi, abdominal region ; cut, cast-off cuticles of previous moults ; cejih, head region ;
in.ij, mid-gut ; o, mouth ; oc.c, compound eye ; prob, rudiment of proboscis of adult ; xtvui, stomodaeum ;
tli, thoracic region ; v.n.c, ventral nerve cord. The crosses mark the boundary between head region
and thoracic region. In A the head region is outlined by a very thick line, the thoracic region by a
line of medium thickness, the abdominal region by a very fine line.

been elucidated chiefly by the labours of Kowalevsky (1884) and
Van Eees (1889). In the first place the larva is a worm-like maggot
or grub, devoid not only of abdominal limbs but of visible thoracic
limbs, of eyes, antennae, and jaws. The region which will form the
head of the fly is represented by a pouch of ectoderm opening in
front (cepli, Figs. 223 A, 224 A), and into this pouch, about half-way
back, the mouth or stomodaeum opens.

Imaginal discs are found on the ventral surfaces of the three
thoracic segments. These consist of pouches of ectoderm connected
with the surface only by strings of ectoderm cells. On the segments
of the abdomen both dorsally and ventrally, there are also imaginal
discs, but these are just areas of thickened ectoderm which are not
invaginated. Finally on the inner surface of the portion of the head

viii AETHEOPODA 279

pouch lying behind aud above the opening of the mouth, there are
two pairs of " tiat " irnaginal discs, the most posterior pair being the
rudiments of the compound eyes, the more anterior the rudiments of
the antennae. Just before the close of larval life a median imaginal
disc is formed in the head pouch, in front and below the mouth,
which is the rudiment of all mouth-parts and of the proboscis of
the fly. From the bottoms of the imagiual " pouches," wings, the
anterior functional and the posterior vestigial, forming the balancers
or halteres, and the legs grow up (Fig. 223, A). As they grow the
pouches enlarge and the strings of cells connecting them with the
ectoderm shorten. At the same time the head pouch also shortens,
its outer portion becoming evaginated so that the opening of the
mouth becomes external, and the imaginal disc for the proboscis lies
posterior.

Then comes the pupal stage. The imaginal pouches now open to
the exterior exposing wings and legs (Fig. 223, C) ; the head pouch
becomes completely evaginated so that the head of the fly is extruded.
The dorsal imaginal pouches of the pro thorax give rise to a stigma with
a bunch of tracheae. The portions of the evaginated pouches surround-
ing the bases of the wings and legs form the adult ectoderm of the
thorax. They spread out till they meet each other. The abdominal
imaginal discs also extend till dorsal and ventral ones meet each
other and right and left discs are united across the middle line. In
this way the larval ectoderm is completely replaced. At the same
time the alimentary canal undergoes profound changes. There is an
imaginal ring of active proliferating cells situated at the inner ends
of both stomodaeum and proctodaeum. The surface of the mid-gut
has " islands " of embryonic tissue dotted over it. By the activity
of these imaginal areas a completely new mid -gut epithelium is
formed, as well as a new lining for stomodaeum and proctodaeum.
The salivary glands have " imaginal rings " situated on their ducts
where these begin to branch. New salivary glands are formed
from the rings on the ducts of the larval glands.

The metamorphosis of most of the higher insects, so far as it has
been studied, is intermediate in character between the types
exemplified by the Chrysomelidae and the Muscid Diptera, and its
real nature is brought out clearly by the researches of Verson (1905)
on the transformations undergone by the alimentary canal of the
silkworm moth, Boinbyx mori. In this case the imaginal discs are
disposed as in Musca — viz. there is a ring at the inner end of the
stomodaeum, a similar ring at the inner end of the proctodaeum, and
a number of islands scattered over the surface of the mid-gut.

Now what Verson clearly shows is that a normal cell which forms
part of the wall of the stomodaeum or proctodaeum, has a limited
life, and, after fulfilling its function for a time and developing its
physiological peculiarities, dies and is replaced by a new cell formed
by the imaginal ring, which is therefore a zone of proliferation. lie
points out further that the formation of both stomodaeum and

280 INVEKTEBEATA CHAP.

proctodaeum iii the embryo, is due to the existence of these zones of
proliferation, and that by their activity in budding off cells external
to themselves they mechanically cause their own invagination. The
cells of the mid-gut likewise have a limited life — they are all
eventually transformed into glandular cells, they exhaust themselves
in elaborating secretion and then die and are replaced by young cells
budded from the imaginal islands.

The great changes which occur at metamorphosis are due therefore
to the fact that a large number of cells terminate their normal
careers simultaneously, and to the fact that a large amount of
proliferation from the formative zones occurs at the same time. But
it is probably true that in animals of all classes, as they grow, the
individual cells forming the tissues wear out and die and are replaced
by young cells lying between the bases of the functional cells — at
least such renewal of tissue is often observed. In some cases, as in
Galerucella, the replacement cell may be a rejuvenated portion of the
original cell, a portion of the nucleus and of the worn-out cytoplasm
being cast off.

Finally, the fact that Arthropoda are enclosed in a rigid cuticle
which is periodically cast off, must lead to this casting off of worn-
out cells and their replacement by new ones being more or less
restricted to the period of moulting — the life-rhythm of the cell
tends, in fact, to be synchronous with the physiological rhythm of
the production of new cuticle ; and so it may be assumed we have in
the metamorphosis merely an intensification of the change that goes
on at every moult. Such critical moults are found in Crustacea also
(see p. 198), and indeed they occur outside the limits of the phylum
Arthropoda altogether, for we have every right to consider the
anmiotic invagination of the Echinopluteus larva to be an imaginal
disc like that of Miisca, and the destruction of larval tissue which
marks the end of their larval life as quite comparable to the histolytic
changes which accompany the metamorphosis of Insecta.

vin AETHKOPODA 281

MYEIAPODA

Classification adopted—

i Pauropoda
Progoneata . . ^ Symphyla

[Diplopoda
Opisthogoneat . . Chilopoda

Before we consider what phylogenetic lessons are to be learnt
from the facts of Insect development which have been set forth in
the preceding pages, we may glance at what is known of the develop-
ment of those lower air-breathing Arthropoda known as Insecta
Myriapoda, in which every segment of the long body bears
appendages, and in which therefore regions corresponding to thorax
and abdomen are not differentiated from one another.

This division constitutes, in fact, a lumber room for forms not at
all closely related to one another, and it is divisible into four
very distinct groups. Three of these — the Symphyla, the Diplopoda,
and the Pauropoda — differ from all Insecta, and from Peripatus also,
in having the genital openings situated in the anterior portion of
the body, not far from the head. They are termed on this account
Progoneata. The fourth group, the Chilopoda or Centipedes, agree
with both Insecta and Peripatus in having the genital opening
situated at the posterior end of the body just in front of the anus,
and are termed on this account Opisthogoneata.

Of the development of Symphyla and Pauropoda nothing is
known. A certain amount of work has been done on the development
of Diplopoda or Millipedes, but the development of a Centipede,
Scolopendra, has been worked out in great detail by Heymons (1901)
and has yielded most interesting results.

SCOLOPENDRA

Scolopendra appears to be quite intermediate in its development
between Peripatus and Insecta, as was to be expected, and there can
be no doubt that in many of its features it represents a stage passed
through by Insecta in their ancestral history. Heynious' main results
concern (a) the segmentation of the egg and the formation of layers ;
(&) the segmentation of the body and the development of the
appendages ; (c) the development of the nervous system ; (W) the
development of the coelom ; and (e) the invaginatiou of the
embryonic rudiment into the yolk, and its subsequent evagination.
We shall say a few words on each of these points in order.

(a) In the earliest stage examined the egg shows an incomplete
division of its substance into columnar peripheral segments which
abut on a central unsegmented portion. This reminds one of the
condition which Eeichenbach found in the eggs of Astacus, which he

282

INVEETEBEATA

CHAP.

nxp

called the formation of primary yolk pyramids, and which he
interpreted as an incomplete segmentation of the egg. Heymons
endeavours to give the same interpretation here, but there are great
difficulties in the way. Thus, in the egg of Astacus each primary
pyramid contains a nucleus in its outer portion, where it is most
sharply marked off from its neighbours, but in ftcolopendra all the

nuclei are contained in the central un-
segmented yolk, and it is more than
doubtful if they correspond either in
number or arrangement with the
pyramids.

The blastoderm in Astacus is derived
from the outermost portions of the yolk
pyramids containing the nuclei, this
portion being cut off from the rest of the
yolk, but in Scolopendra the blastoderm
originates as in Insecta, through the
migration of nuclei from the centre to
the periphery of the egg. These nuclei
are surrounded by bodies of cytoplasm
forming " free cells," as they may be
termed, and they migrate outwards
between the adjacent pyramids. It is
clear, therefore, that the pyramids iu
Scolopendra have no relation to the
division of the egg into blastomeres, but
.prod are a phenomenon of the same kind as
we met with in the egg of the Spider,
the peculiar yolk-rosettes of which are
FIG. 225.— Ventral view of the quite unconnected with the true seg-

embryonic area in a developing mentation.

of Scolopendra cengulata.
(After Heymons.)

If we eliminate the yolk pyramids
the formation of the layers is almost

nut, antenna; aiin, appendages of • -, , • • cv 7 ^ T •

the body ; c.i, caudal lobe ; lab, labrum ; identical in Scolopendra and Lepism a.

The endoderm is budded off from a thick-
ened area of the blastoderm termed bv

•nt n, mandible; i/u'1, first maxilla ; ma.2,

second maxilla ; «/r;i, maxilliriede

(poison-claw); o, mouth ; pr.ant, pre- . . .

antenna; pwt, opening of proctodaeum. HeymOllS the "CUmulUS priHlltlVUS, Dllt

which we might more appropriately term

the primitive streak ; the cells which ultimately form the endo-
derinal epithelium and those that form yolk cells are indistinguishable
from one another ; the mesodermic bands arise from the hinder
border of the cumulus and extend forwards, and their extent defines
the embryonic area as in Insecta.

(6) The division of the body into segments and the outgrowth
of the appendages therefrom occurs as in Insecta. There is an
intercalary segment which, however, develops no appendages ; there
are three jaw segments, behind which comes the segment bearing
the powerful poison claws characteristic of Chilopoda. But in

viii ARTHKOPODA 283

Scolopendra a segment is developed in front of the antennae
on which are a pair of rudimentary appendages, the prae-antennae
(pr.ant, Fig. °2'2^). No such segment and no such appendages have
been detected as yet in any other Arthropod, unless the rudimentary
antennae which have been described in the embryos of certain
spiders be homologous with them.

It will be remembered that Kishinouye describes a pair of
coelomic sacs in the head region of Limidus and spiders ; now the
true prae-oral region or acron of Insecta never possess coelomic
sacs. It is therefore possible that these prae-oral coelomic sacs of
Arachnida may be the remnants of a lost prae-chelicerau segment
corresponding to the prae-autenna.

The ectoderm covering each segment is thickened in two places
on each side, one immediately above the insertion of the limb which

J fj

Heymous regards as the rudiment of the tergum, and one below the
insertion of the limb which he regards as the sternum. The two
terga are separated by a thin dorsal membrane, and the two sterna
by a thin sternal membrane. This tritid division of the dorsal covering-
is indicated in a later stage, when chitin has been developed, by two
longitudinal furrows which mark out the dorsal sclerites into three
regions, and Heymons regards it as a reminiscence of a, TriloHte ancestry
for the Centipedes, and through them for the whole of the Insecta.

(c) The nervous system develops as two bands of thickened
ectoderm underlying the coelomic sacs and separated by a median
groove. These bands are thickened in each segment, and these
thickenings constitute the ganglia. In each ganglion there is an
ectodermic pit, which owes its origin to the energy with which, at
these spots, cells are proliferated towards the interior to constitute
the nerve cells. The pits eventually become closed in and with-
drawn from the surface ; their outer walls do not become nerve cells
but form a sheath enveloping the ganglion. From the mid-ventral
membrane a string of cells is split off which, by contraction, gradually
draws right and left ganglia together.

The brain consists of an archicerebrum, or original pair of supra-
oesophageal ganglia in the acron, and of two pairs of lateral pits, a
more median and a more lateral pair. These pits give rise to
ganglionic masses which increase the size of the original ganglion in
the acron. The small optic lobes are developed from the lateral pits.
The compound ganglion so formed is known as the protocerebrum.
The ganglia of the antennary region give rise to the deuterocerebrum,
those of the pre-antennary segment to the bridge connecting proto-
and deuterocerebrum. The ganglia of the intercalary segment give
rise to the tritocerebrum. Since the deuterocerebrum of Crustacea
resembles in its structure the deuterocerebrum of Insecta and Myria-
poda Heymons concludes that the two are homologous, that conse-
quently the antennae of Insecta correspond to the antennules "f
Crustacea, and that the prae-antennae of ,SVW^o/<//v/ and the segment
from which they spring have been entirely suppressed in Crustacea.

284 INVEKTEBRATA CHAP.

(d) The coelom is developed in the same way as in Insecta, and
is eventually occluded by the transformation of the cells forming its
walls into a fat-body. But before this happens each coelomic sac
becomes divided by folds into three portions — a dorsal, a lateral, and
a ventral. The first gives rise to the wall of the heart, the pericardial
septum, and the genital tubes, as in Peripatus and Insecta. The
lateral gives rise to muscles and to certain strings of " lymphoid
tissue," and, in the region of the intercalary segment, to two masses
lying at the sides of the oesophagus ; these are all regarded by
Heymons as the degenerate remains of " nephridia " like those of
Peripatus. The ventral sections of the coelom, unrepresented in
Peripatus, extend towards the middle line, and from their adjacent
walls the walls of the ventral vessel are formed. In the genital
segment the lumen of the coelom remains undivided and forms the
proximal section of the genital duct, leading from the tubular genital
organ above towards the genital opening below, as in Peripatus.

(e) The embryonic area of Scolopendra, marked out by the
appendages and underlying somites, grows in length till it extends
more than half-way round the egg. Then it is bent into a V shape
by a transverse furrow, and infolded into the egg. During this
process the two mesodermal bands become widely separated in the
middle, meeting one another only at the anterior and posterior ends,
and the yolk comes into contact with the much-stretched ventral
ectoderm. Eventually, when most of the yolk has been absorbed,
the embryonic area is straightened out again.

By this account we are forcibly reminded both of the early stages
in the development of the spider, especially of the process called
" reversion," and of the early development of Machilis. But there
are certain great differences between Machilis and Scolopendra. In
the latter, practically all the much-stretched dorsal ectoderm is.
eventually incorporated into the adult ectoderm or " hypodermis " ;
but in Machilis a large portion of the dorsal ectoderm undergoes the
peculiar histological change described above, and forms " serosa " which
is later enfolded into the yolk as the dorsal organ, it degenerates and
is digested, and the dorsal " hypodermis " is largely formed by an
extension upwards of the ectoderm at the sides of the embryonic
area. Nevertheless, in Scolopendra a small portion of the dorsal
ectoderm in the neck region thickens and forms a dorsal organ. The
cells forming it degenerate and are absorbed, so that in it we have
the first rudiment of a " serosa."

What little is known of the development of Diplopoda or
Millipedes need not detain us long. We owe most of the knowledge
we possess to Metschnikotf (1874), and to Heathcote (1886 and
1888). It appears that the segmentation of the egg agrees closely
with that of Scolopendra. Metschnikoff (1874) describes a division
of the surface into radial pyramids, and a conglomeration of nuclei in
the central portion. The ovary of Julus is a wide sac beneath the
gut, on the walls of which are two bands of germ cells. This sac,

vin AETHEOPODA 285

according to Heathcote (1888), originates by the fusion of the
ventral portions of coelomic sacs, and is in fact a remnant of tin;
coelom. The mid-gut epithelium is formed by an accumulation of
yolk cells, not, as in Scoloiicndra, on the surface of the yolk, but in the
form of a string traversing its centre. It follows that as development
proceeds the yolk is situated, not in the cavity of the gut, but in the
body-cavity, so that between Diplopoda and Chilopoda there is the
same difference as between Gnathobdellidae and Ehyncobdellidae
among Leeches.

The embryo is hatched as a larva, when, in addition to jaws, it has
only three pairs of legs. Additional legs are added in subsequent
moults. Scolopendra, on the contrary, is hatched with all its
appendages developed, and this is true of many Centipedes which are
termed on this account Epimorpha. But there are many Centipedes
which agree with the Millipedes or Diplopoda in being hatched with
an incomplete number of segments. Such forms are termed
Anamorpha.

GENERAL CONSIDERATIONS ON THE ANCESTRAL HISTORY OF ARTHROPODA

We may now review the whole of the facts which we have learnt in
order to see what light they throw on the relationships of the Insecta,
Myriapoda, and Hexapoda, and the Onych.oph.ora. Since in their
embryonic development most insects pass through a stage where
appendages are developed on the segments of the abdomen, and since
in the lowest Insects such appendages persist in a rudimentary form
throughout life, there is no doubt that Insecta Hexapoda are derived
from Myriapoda ; and since, like Scolopendra and Peripatus, they
have the genital opening situated at the hinder end of the body, they
must be derived from some opisthogoneate stock like the Chilopoda,
rather than from progoneate forms.

To find the origin of these last named we must go back to an
ancestral condition where there were many genital openings on each
side of the animal, a condition retained only in some Pantopoda, and
one in which the ancestors of Myriapoda cannot have made much
advance beyond that found in Polychaeta.

It is a tempting hypothesis, however, to suppose that such a
state may have existed in the extinct Trilobita. In this group
there was more uniformity in the character of the appendages borne
by the various segments than in any other long-bodied Arthopod, and
moreover they agreed with Insecta, Myriapoda, and Onychophora in
possessing a single pair of antennae as prae-oral appendages.

If this hypothesis be accepted we should be dealing, in the case
of Insecta, in the broad sense, with a land branch of a stoc.k which
we know to have been dominant in the seas of the Cambrian and
Silurian epochs. The Onyr.hophora would then be a, somewlmt
degenerate offshoot from the base of this stem, degenerate in the
thinness of its cuticle and in the loss of distinct joints in its

286 INVERTEBRATA CHAP.

appendages, primitive in most other respects, and preserved up to
the present day in consequence of its secluded and burrowing habits.
The Diplopoda and other Progoneates would represent another
degenerate offshoot, whilst the Chilopoda and Insecta Hexapoda
would constitute the main stem.

The land Arachnida may plausibly be regarded as later invaders
of the land. They, too, are connected with the Trilobite stem, but
more remotely, for in them a differentiation between prehensile and
ambulatory legs in front and blade -like respiratory appendages
behind, had been effected before the ancestral Arachnid left the
water. Crustacea can also be directly traced back to primitive
Trilobita ; indeed the Nauplius larva, as we have already seen, is
in one sense the repetition of the Trilobite stage in Crustacean
ancestry.

The main difficulty connected with this hypothesis concerns the
origin of the compound eye. Since Peripatus, Myriapoda, the lower
Insects, and the larvae of the higher Insects, agree in possessing only
simple pit-like ocelli, it is fairly clear that the massing together of
these ocelli to form a compound eye must have occurred during
the evolution of the Arthropodan stock, and had not occurred in
the primitive land Arthropoda. But primitive Crustacea, primitive
Arachnida, and most Trilobita possess compound eyes. The Insecta,
therefore, must have been derived from primitive Trilobita in which a
compound eye had not yet been developed, and, considering that a fully
formed Orthopteran insect is already found in Silurian strata, this is
what we might naturally expect.

One suggestion may be made here of a possible future line of
research, though it must be understood it is merely an indication
of such. In Trilobita, primitive Arachnida, and very many Crust-
acea, the compound eye is carried on a lateral projection of the
prae-oral region, and in the higher Decapod Crustacea this be-
comes a movable appendage. In shrimps, when this appendage
is cut out along with the optic ganglion it is regenerated, not as
an eye, however, but as an antenna-like organ. The question is—
Is it possible that in the compound eye of Trilobita, Crustacea,
and Arachnida we have the representative of the prae-antennae
of Scolopendra, and that the compound eye of Insects has had
an independent origin ? This is a subject which is well worth
investigation.

Before leaving the subject of the Insecta, however, another very
difficult problem, and one of fundamental importance for embryo-
logical science, presents itself, and that is the question — What
significance are we to attach to the larval phases of Insects ? We are
confronted with the extraordinary circumstance that the lowest insects,
like Machilis, Lepisma, etc., are hatched from the egg in practically
the adult condition ; that the more primitive groups of winged
Insects, like Orthoptera, Odouata, etc., emerge from the egg in a
condition fundamentally like the adult, except for the absence of

vin ARTHROPOD A 287

wings ; and that in the most modified Insecta a worm-like larval
stage is found.

Now we have proceeded on the assumption, which all the clearest
cases seem to warrant, that the larva always represents, with more or
less physiological modification, an ancestral condition of the stock.
Why, therefore, should the lowest branch of the Insecta fail to show
this larval stage more clearly than the highest and most modified
branch ? Is it possible that a larval stage may be secondarily inter-
calated in a life-history in which the young were originally hatched
with all the adult characters ? Such considerations force us to look
at Insect larvae a little more closely from another point of view.

Now we find that the caterpillar form of larva, with biting mouth-
parts and abdominal appendages on some of the segments, crops up
not only in Lepidoptera, but also in the more primitive Hymenoptera ;
but in the former case the appendages are borne on segments 2, 3, 4, 5,
and 10 of the abdomen, and in the latter case on segments 3, 4, 5, 6,
7, 8, and 10. Again an adult form with biting mouth-parts and rudi-
mentary abdominal appendages, which, as a matter of fact, are used
to assist in locomotion, is found amongst the Thysanura, as, for
instance, in Machilis. We conclude, therefore, that the caterpillar,
or eruciform type of larva, represents a Thysanuran ancestor, and
the reason why the Thysanura do not exhibit this phase in the
earlier portion of their life-history is that it represents their adult
condition.

But just as the primitive type of Echinoderrn larva, found amongst
Asteroidea, has undergone modification and reduction amongst the
more modified groups of Ophiuroidea, Echinoidea, and Holothuroidea,
so the eruciform type has undergone modification and reduction in
other types of higher insects, till it becomes, in extreme cases, a legless
" grub," as in Muscidae. Where the mother, in consequence of her
improved powers of flight and her developed senses and instincts, is
able to provide her offspring with a store of nourishment which does
not require much mastication, and which ensures there shall be
demand for little or no active exertion on the part of the offspring to
gain food, then not only will abdominal appendages disappear, but
also the thoracic appendages, and even the gnathites or jaws. In fact,
we then have influences acting on the larvae similar to those which
have produced legless and senseless parasites from adult forms in
other groups of the animal kingdom.

It must be admitted that this explanation will not fit the case of
Coleopterous larvae, many of which are quite active, but which do
not develop abdominal appendages. There must be some independent
reason for the suppression of these appendages in the larva which
still may appear in the embryo (Melolontlia), but which may be sup-
pressed even there (Uonacia').

The lower winged insects, often termed from the absence of a
pupal stage in their development Hemimetabola, pass through the
stage corresponding to the caterpillar, within the egg membrane ; as

288 INVEETEBRATA CHAP.

»

the embryo of Blatta, with its well-developed abdominal appendages,
abundantly proves. The so-called nymph, which emerges from the
egg without wings, or with mere rudiments of them, corresponds to
the pupal stage of higher insects, the difference being that the nymph
is active and seeks its own food.

The reason why the caterpillar stage has become embryonic in
the lower insects is probably closely akin to the reason why the
development of the egg in an extremely primitive form like Peripatus
takes place entirely within the maternal body. It may perhaps be
expressed by a single phrase, " the pressure of modern competition."
The caterpillar-like form of larva would not stand the remotest chance
of survival unless the mother sought out for it a suitable environ-
ment, with plenty of food near at hand and easy to get. Where the
mother has not sense enough to do this, either the stock must die
out or the corresponding stage must be passed over within the egg
membrane.

The active nymph which emerges from the egg is hard enough
put to it to survive. In the case of Odonata and Epherneroptera, to
take instances, it is driven to seek shelter in an aquatic life, and may
be driven to develop organs like tracheal gills, which bring oxygen
to the tissues by extracting it from the water and passing it by
diffusion into air-tubes deprived of external openings, and from these
to the blood — a roundabout plan which betrays the secondary nature
of the aquatic life of these nymphs.

In general it may be said, that since the invention of birds and
bats the life of a winged insect has become a much more perilous one
than formerly, and to this circumstance we attribute the fact that
there is a strong tendency to shorten the life-period of the imago and
prolong that of the larva. Indeed it often occurs that the imago takes
no food, or, as in all Lepidoptera, only food which is incapable of
prolonging life, since it is but saccharine. In the same way and for
the same reason, when sex union and egg-laying are accomplished, the
imago dies, no matter how securely it may be screened from enemies.

The larval stage of Insecta, therefore, agrees in its fundamental
nature with the larval stages of other animals, and, we may be assured,
has not been secondarily intercalated in the life-cycle : it represents a
Thysanuran ancestor, but in the majority of insects it has undergone
great secondary modification, and in the so-called Hemimetabola,
like Orthoptera, it has become embryonic, and is passed through
while within the egg membrane.

LITERATURE REFERRED TO

PUOTOTRACHEATA

Sedgwick, A. The Development of the Cape Species of Peripatus. Quart. Journ.
Mic. vSnc., vols. 25-28, 1885-1888.

Sheldon, L. On the Development of Pfripalus novae-zelandiac. Quart. Journ. 51 ir.
Soc., vols. 28-29, 1888-1889.

vni ARTHROPOD A 289

CRUSTACEA

Balfour, F. A Treatise on Comparative Embryology. London, 1881.

Bigelow, M. The Early Development of Lepas : a Study of Cell-lineage and Germ-
layers. Cont. Zool. Lab. Mus. Comp. Zool. Harvard, No. 132, 1902.

Brooks, W. K. Lucifer, a Study in Morphology. Phil. Trans. Roy. Soe., vol. 173B,
1882.

Caiman, W. A Treatise on Zoology, edited by Sir E. R. Lankester, vol. 7, fascicle 3.
The Crustacea. London, 1909.

Glaus. Zur Anatomie nnd Entwicklungsgesohichte der Copepoden. Arch.
Naturgesch., vol. 24, 1858.

Glaus. Untersuchungen zur Erforschung der genealogischen Grundlage der
Crustaceensystems. Vienna, 1878.

Dohrn. Die Uberreste des Zoaea-Stadiums in der ontogenetischen Entwicklung
der verschiedenen Crustaceen-Familien. Jen. Zeit. Naturgesch., vol. 5, 1870.

Groom, T. T. The Early Development of Cirripedia. Phil. Trans. Roy. Soc.
Lond., vol. 185, 1894.

Hatschek. Beitriige zur Entwicklungsgeschichte der Lepidopteren. Jen. Zeit.
Naturgescli., vol. 11, 1877.

Hatschek. Studien zur Entwicklung der Anneliden. Arb. Zool. Inst. Wien,
vol. 11, 1878.

[These two papers by Hatschek are cited here because they contain references to
the significance of the Nauplius.]

Korschelt und Heider. Lehrbuch der vergleichenden Entwicklungsgeschichte der
wirliellosen Thicre, Jena, vol. 1, 1890.

Kiihn, A. Die Sonderung der Keimbezirke in der Entwicklung der Sommereier
von Polyphemus pediculus. Zool. Jahrb., Abt. fiir Anat., etc., vol. 53, Heft 2, 1912.

Lister, J. J. Note on a (? Stomatopod) Metanauplius Larva. Quart. Jonrn.
Mic. Sc., vol. 41, 1898.

Morin. Zur Entwicklungsgeschichte des Flusskrebses. Sitzungsber. Neuruss.
Ges. Odessa, vol. 11, 1886.

Muller, F. Fiir Darwin. Leipzig, 1866.

Reichenbach. Studien zur Entwicklungsgeschichte des Flusskrebses. Abb.
Senckenberg. Naturforsch. Ges. Frankfurt, vol. 14, 1888.

Sars, G. Bidrag till Kundskaben oin Decapoderns Forwandlingen. Arch. Math.
Naturvidenskab Christiania, vol. 14, 1891.

Taube. Beitiiige zur Entwickltmgsgeschichte der Euphausiden. Zeit. fiir wiss.
Zool., vol. 92, 1909.

Wilson. North American parasitic Copepoda (Lernaeopodida). Proc. U.S.
Nat. H. Mus., vol. 39, 1911.

ARACHNIDA

Beecher. On the Thoracic Legs of Triarthrus. Amer. Journ. Sci., vol. 46, 1893.

Brauer. Beitrage zur Kenntniss der Entwicklungsgeschichte des Skorpions.
Pt. I. Zeit. fiir wiss. Zool., vol. 57, 1894; Pt. II. ibid., vol. 59, 1895.

Kautsch, G. Uberdie Entwickluug von Agelcna, labyrinthica. Pt. I., Zool. Jahrb.
Abt. fiir Anat., vol. 28, 1909 ; Pt. II., ibid., vol. 30, 1910.

Kingsley. The Development ofLimulus. Journ. Morph., vol. 7, 1892; vol. 8, 1893.

Kishinouye. The Development of Araneina, Journ. Coll. Sc. Imp. Univ. Tokio,
vol. 4, 1891 ; The Development of Limulus lonyispina, ibid., vol. 5, 1893 ; On the
lateral eyfss of the spider, ibid., vol. 5, 1893 ; Note on the Coelomic Cavity of the
Spider, ibid., vol. 6, 1894.

Patten. On the Origin of Vertebrates from Arachnida. Quart. Journ. Mic. Sc.,
vol. 31, 1890.

Purcell, W. The Development and Origin of the respiratory Organs in the Araneae.
Quart. Journ. Mic. Sc. , vol. 54, 1909.

Schimkewitsch. Uber die Entwicklung von T//I-/I////IOIIHS <-«ii</nftis. Zeit. fiir
wiss. Zool., vol. 81, 1906.

I'ANTOroDA

Morgan, T. H. A Contribution to the Embryology and Phylogeny of the
Pycnogonids. Studies Biol. Lab. Johns Hopkins Univ., Baltimore, vol. 5, 1891.

VOL. I U

290 INVERTEBBATA CHAP, vm

TAUDIGRADA

Erlanger. Beitrage zur Morphologie der Tardigrade:!. Zur Embryologie eines
Tardigraden Mucroliotus macronyx. Morph. Jalirbuch, vol. 22, 1895.

INSECTA

Gunther, K. Die Sehorgane der Larve und Imago von Dytisctis marginal-is.
Zeit. fur wiss. Zool., vol. 100, 1902.

Hirschler. Die Embryonalentwicklung von Donacia crass-ipcs. Zeit. fur wiss.
Zool., vol. 92, 1909.

Heymons. Die Entwicklung der weiblichen Geschlecbtsorgane von Phyllodromia
(Blatta} gcrmanica. Zeit. fur wiss. Zool., vol. 53, 1891.

Heymons. Uber die Bildung der Keimblatterbeidenlnsecten. Sitzungsber. Kb'nig.
Preuss. Akarl. AViss., vol. 1, 1894.

Heymons. Entwicklungsgeschichtliche Untersuchungen an Lcpisma saccJutri/ni.
Zeit. fur wiss. Zool., vol. 62, 1897.

Heymons. Die Entwicklungsgeschichte von Machilis. Verb. Deutscb. Zool. Gesell
15 tb year, 1905.

Kowalevsky. Beitrage zur nacbembryonalen Entwicklung der Musciden. Zool.
Ann., vol. 8, 1884.

Poyarkoff. Recbercbes histologiques sur la metamorphose d'un Coleoptere.
Arcb. d 'anatomic microscopique (Paris), vol. 12. 1910.

Tower. Tbe Origin and Development of tbe Wings of Coleoptera. Zool. Jabrl>. ,
vol. 17, 1909.

Van Rees, J. Beitriige zur Kenntiiiss der inneren Metamorpbose von Muscu-
vomitorin. Zool. Jabrb., Abt. fur Anat. , vol. 3, 1889.

Verson. Zur Entwicklung des Verdauungs-Kanal bei Bombyx mori. Zeit. iiir
wiss. Zool., vol. 82, 1905.

Wbeeler, W. M. Tbe Embryology of Blatta gcrmanica and of Doryphora dcccm-
lincata. Journ. Morpb., vol. 3, 1889.

MYUIAl'ODA

Heathcote. Tbe Early Development of Julus tcrrestris. l^uart. Journ. Mie. Sc. ,
vol. 26, 1886.

Heathcote. Tbe Post-embryonic Development of Julus tcrrestris. Pbil. Trans.
Roy. Soc. (London), vol. 179, 1888.

Heymons. Die Entwicklungsgescbicbte der Scolopender. Zoologica, Heft 33, 1901.

Metscbnikoff. Embryologie der doppelfiissigen Myriapoden. Zeit. fur wiss. Zool.,
vol. 24, 1874.

CHAPTER IX
MOLLUSCA

Classification adopted —

Solenogastres

f Isopleura Polyplacophora

Gastropoda I Prosobranchiata ' Aspidobranchiata

I J. J. VkJW WJ. CV A A V-AJ.ACH UCV i -_- * . - 1 • j

. • , L~ . ., , , . iPectmibrancniata
[Anisopleura Opisthobranchiata

[Pulmonata
Scaphopoda

Pelecypoda (Lamellibranchiata)
Cephalopoda

ONE of the most surprising facts brought to light by the study of
embryology is the near affinity of the Mollusca and Annelida. The
adult structure in the two groups is widely different, but in their
early development Mollusca and Annelida correspond almost cell for
cell. The credit of having proved this important fact, by the most
elaborate and laborious researches, belongs to the American School of
Zoologists. Conklin's ( 1897) monograph on the development ofCrepidula
may be regarded as the foundation of our knowledge on this subject.
A Polish zoologist, Wierzejski (1905), has, however, made the most
complete study of the cell-lineage of a Mollusc as yet published. He
worked on Physa, but Physa is unfortunately a form whose develop-
ment is very much modified, and hence is not suitable as a type for
special description. On the other hand, the common limpet, Patella,
exhibits a most primitive type of development, and it is found all
round the British and European coasts in countless numbers, and
allied genera are common on the coast of America. The development
of the Mediterranean species, Patella coerulea, has been investigated
by Patten (1885) and E. B. Wilson (1904), and we therefore select
it as a type for more special study.

PATELLA

There is no reason to believe that the development of the British
species, Patella vulgata, differs in any important respect from that

291

292 INVEETEBEATA CHAP.

of P. coerulea, and the eggs of the British species can be artificially
fertilized and the larvae reared through their complete development
on a diet of the diatom Nitschia.

According to Wilson, the eggs of Patella coerulea are found ripe
from March until June ; the eggs of the British species, on the
contrary, appear to ripen in October and November. The ripe eggs
are surrounded by a " chorion " ; this membrane, however, gradually
dissolves when the eggs are allowed to stand in sea- water. Artificial
fertilization is greatly assisted if both eggs and sperm, before being
brought together, are allowed to lie in sea-water which has been
rendered slightly alkaline by the addition of from 4 to 6 drops of
a 5 per cent solution of caustic soda to every 500 cc. of sea-water used.
In many cases more than one spermatozoon penetrates the egg and
abnormal development results, but these abnormally fertilized eggs
are recognizable from the fact that they divide at the first cleavage
into four blastomeres instead of into two only, as normally fertilized
eggs do. If, therefore, at the time of the first cleavage, the eggs
which have divided into two blastomeres only are picked out with
a fine pipette, a supply of normally fertilized eggs will be obtained
whose further development can be studied in detail.

For his studies in cell-lineage Wilson preserved the cells simply
in acetic acid. To a watch-glass full of sea-water containing the eggs
a few drops of glacial acetic were added, and then, drop by drop,
dilute glycerine. After a short interval, when a sufficient quantity
of dilute glycerine had been added, strong glycerine was added in the
same way. The eggs were in this way slowly transferred to a medium
of thick glycerine, in which they were studied ; they thus became
absolutely transparent, whilst the cell boundaries showed up as dark
lines, so that the segmenting egg looked like a glass model. A slight
trace of stain with acid carmine is sometimes an improvement, but
in most cases Wilson considers its use superfluous. It must be
remembered that preparations made in this way are not permanent,
but they afford more insight into the cell -lineage than those
obtained by any other method.

The egg divides into two and then into four completely equal
cells, and thus it is almost impossible to discriminate the quadrants
of the egg from one another. This is quite impossible when the four
first blastomeres meet quite evenly in the axis of the egg. But for
four semi-fluid masses to meet in a single vertical line of junction is
an impossibly unstable condition ; they either meet so as to leave a
vertical space between them, their inner angles being somewhat
rounded off, or else they meet so as to form a " cross furrow " at one
or both poles. By a cross furrow is meant the meeting of two of the
blastomeres along a short surface so as to separate the other two from
each other. If a given two, say B and D, meet thus at the vegetative
pole of the egg, then the other two, A and C, will similarly meet at
the animal pole of the egg, so that two short " cross furrows " at right
angles to each other are thus produced.

IX

MOLLUSCA

293

Now, as a result of the study of eggs with spiral cleavage belonging
to many different species, it has been found that in all cases of normal
cleavage — i.e. where D is the left posterior macromere — the cross
furrow at the vegetable pole slants upwards from left to right when
looked at from above, the inacromeres being placed in their normal
position. But we can determine what is their normal position from
the fact that the polar bodies are given off from the animal pole, and
if we then look at the egg from this pole and rotate it until the cross
furrow takes up the proper position, we know that the left anterior
blastomere is A, the right anterior B, and so on (cf. Fig. 226). The
cross furrow does not always

appear in the early stages in io\ _ i / P

v 4 u j T_ -.L j - ' V^ ^r>^^^lo2

Patet/a, and when it does not,

it is impossible to be sure of
the orientation of the egg.

The 8 -cell stage is reached
as usual by the fourth cleavage,
and in it the four upper
cells or the first quartette
of micromeres are decidedly
smaller than their lower sisters
the niacrorneres (Fig. 226). The
micromeres are separated from
the inacromeres as usual by
the formation of dexiotropic
spindles.

At the next cleavage the
first-formed micromeres divide
by laeotropic spindles into a
set of cells, Iq1, above, and a
set, Iq2, below. The cells de-
noted by the symbol Iq2 are

slightly larger than those named Iq1. At the same time the inacro-
nieres also divide laeotropically, giving rise above to . the second
quartette of micromeres. These micromeres are larger than the first
quartette, but still much smaller than the residual rnacromeres 2 A,
2B, 20, and 2D.

At the next cleavage the 32-cell stage is attained. Each of the
basal cells 2A, 2B, 20, and 2D divides dexiotropically so as to give
rise above to a small daughter cell. These four smaller cells
constitute the third quartette of micromeres, and, as in Annelida,
the three quartettes give rise to all the ectoderm. The second
quartette cells divide, at the same time, each into two almost equal
daughter cells. The lower daughter cells derived from the first
quartette Iq2 divide quite equally into upper cells Iq21 and lower Iq22.
As in the eggs of Polygordius, all the descendants of Iq2 enter into the
formation of an equatorial band of ciliated cells — or prototrochal
girdle, which later encircles the larva about its equator. The

FIG. 226. — Development of Patella coerulea.
8-cell .stage showing the spindles preparatory
to the formation of the 16-cell stage. The
spindles in the upper cells show the laeo-
tropic twist. (After Wilson.)

i'.f, cross furrow at the vegetable polfl ; pJ>, polar
bodies.

294

INVEETEBEATA

CHAP.

121

122

uppermost cells of the egg, Iq1, divide into larger daughters, lq12,

below and very small
daughters, lq11, above,
which occupy the ex-
treme animal pole of
the egg.

The egg up

11

221

till now

is perfectly radially sym-
metrical, and no differ-

221 ence whatever can

212

be

its
in
the

B

the

belong

four arms
to the

detected between
different quadrants
this respect. With
sixth cleavage, however,
leading to the formation
of the 64-cell stage, this
radial symmetry is lost,
and is replaced by a
bilaterally symmetrical
arrangement.

The divisions which
constitute this cleavage
are as follows. The cells
lq11 divide in regular
spiral order into cells
lq111, which correspond
to the apical cells of
Polygordius, and into
lq112, the peripheral ros-
ette cells, which corre-
spond to the Annelidan
cross in the larva of
Polygordius. The cells
lq12 also divide spirally
into daughters of equal
size, and give rise to the
so-called Molluscan
cross, which at this stage
has curved arms. The
upper daughters, lq121,
form what are called the
basal cells of the cross ;
the lower daughters,
lq122, constitute the
intermediate cells of
the cross, but the tips of
are constituted by the four tip cells, 2qn, which
second quartette of niicromeres. The cells lq21

112

FK;. 227. — Two stages in the development of the upper
hemisphere of the embryo of Patella coerulea viewed
from above. The primary trochoblasts are un-
shaded. The cells belonging to the second quartette
are dotted, those forming the Molluscan cross are
ruled with horizontal lines, whilst those forming
the Aunelidan cross are covered with small circles.
The apical cells are unshaded. (After Wilson, some-
what altered. )

A, stage in which the cells forming the Jlolhiscan cross
are undrrnoing tln'ir lirst division. B, stage in which the cells
forming the; Mollnscan cross are dividing for the second time,
and in which the cells forming the Annelidan cross have
appeared.

IX

MOLLUSCA

295

and lq22 also divide into equal daughters, and give rise, as in
the larva of Poli/gordius, to four lozenge -shaped groups of four
cells. These sixteen cells are termed the primary trochoblasts
(Fig. 227, Iq211, lq212, lq221, lq222).

The cells of the second quartette of rnicroineres divide as follows :
2qx divides into the tip cells 2qu, which alternate with the four groups
of primary trochoblasts, and into four lower cells, 2q12. The cells 2q2
divide into four larger upper cells, 2q21, and four smaller lower cells,
2q22, situated near the vegetative pole of the egg. The cells 2q21 are
situated nearly side by side
with 2q12.

Of the cells of the third
quartette 3a and 3b divide
spirally like all the cells
we have so far mentioned,
giving rise to 3aa and 3a2,
3bT and 3b2, respectively ;
but 3c and 3d divide by
spindles so directed as to
converge tomti-nh the median
plane of the embryo and
make equal tingles with it;
* i nd this division constitutes
the first appearance of 'bi-
lateral symmetry in the egg
(Fig. 228), which lias now

assumed the form Of a hollow FlG< 228. _ Stage in the development of the

blastula.

The residual macromere
3D glides upwards into the
blastocoele, remaining for
a time in connection with
the surface by a narrow
neck ; it then divides into
an internal cell, 41), which
will form part of the mid-

embryo of Patella coentlcii, showing the first
division of the third quartette and the beginning
of bilateral symmetry seen in the direction of
the spindles in 3e and 3d. Viewed from the
vegetative pole of the egg. The apparent small
size of the macromere 3D is due to its movement
inwards, which is the beginning of the process
of gastrulation. The cells of the third quartette
are ruled with vertical lilies. Those of the
second quartette are dotted. The residual
macromeres are white. (After Wilson, some-
what altered.)

gut, and into a superficial
cell, 4d, which is the mother cell of the mesoderm. This
gliding upwards of 3D, which we can only attribute to altered
cytotaxis, is the first sign of the process of gastrulation (Fig. 229).
The other macromeres, 3A, 3B, and 30, then, a little afterwards,
follow the example of 3D and migrate inwards, also remaining for
a short time in connection with the surface by long necks. Then
they also divide ; but, in the case of each of these, both their
daughters form part of the wall of the mid-gut.

As development proceeds further, divisions take place amongst
the apical cells, in the rosette cells, and in the cells of the Molluscan
cross. The cells of the Annelidan cross divide only once more.

296

INVEETEBEATA

CHAP.

The division of the apical cells Iq111 results in the formation of a well-
marked plate of eight central cells at the animal pole (Fig. 231).

B

D

3D

FIG. 229. — Two stages in the gastrulation of Patella coerulea in optical longitudinal section.
The residual macromeres are shaded. (After Wilson. )

A, stage showing the formation of the mesoderm mother cell, 4(7, and the inward migration of the
macromere, 3D. B, stage showing the division of the left nu-soderm mother cell, and the inward
migration of the other macromeres. ap, apical plate ; ji.tr, prototroch.

Meanwhile other
changes take place. The
four groups of primary
trochoblasts develop
transverse rows of power-
ful cilia, each row bearing
a striking resemblance
to a single "comb" of
a Ctenophore, and the
apical cells develop a
terminal tuft of long
stiff cilia. The embryo
at this stage, when looked
at from above (Fig. 230),
bears a striking resem-
blance to a larval Cteno-
phore ; and this stage,
which is reached eight
hours after fertilization,
is termed by Wilson the
Ctenophore stage.

The cells constituting the apical plate do not appear to divide
further, but the cells forming the arms of the Molluscan cross under-
go repeated divisions, in consequence of which these arms cease to be

1221

FIG. 230. — The " Ctenophore " stage in the development
of J'nti-Uii cni'i-iileii. Seen from above. The cells
are marked as in Fig. 227. (After Wilson, somewhat
altered.)

IX

MOLLUSCA

297

distinguishable from one another, all four constituting a mass of
small cells covering the upper hemisphere of the egg (Fig. 231).

The ectodermic cap of micromeres extends downwards so as almost
to reach the vegetative pole
by the process of growth
known as epibole (see p. 72),
and thus, by epibole, the
process of gastrulation is
completed. For a time a
small opening persists at
the vegetative pole, where
the rnacronieres are un-
covered by micromeres, and
this is the blastopore.

In the meantime the
mother cell of the meso-

derm (4d) has become
divided into right and left
The proto-

daughters.

trochal girdle has now

ap

FIG. 231. — View of the upper hemisphere of an
embryo of Patella coerulea just before hatching.
(After Wilson.)

<i/i, apical cells ; p.tr, prutotrochal cells.

acquired the form of a
complete circle through
the acquisition of cilia by
those cells which intervene between adjacent groups of primary
trochoblasts. These cells may be termed secondary trochoblasts,
and two of them in each quadrant are derived from the first

quartette ; they are in fact
daughters of the outer cross
cells lq122. One secondary
trochoblast in each quadrant
P£ is derived from the second
?" quartette; these are the tip
cells of the arms of the
Molluscan cross, 2qn : and in
this way the number of cells
entering the prototrochal
girdle is raised by three in
each quadrant, making a total
of 28 (16 + 12). Occasionally

FIG. 232.— Lateral view of a late embryo of Patella the tip Cell divides into two,

and then there are 32 second-
ary trochoblasts. The cilia
borne by the secondary trocho-
blasts are at first much
shorter than those borne by
the primary trochoblasts (Fig. 232). By secondary shif tings these cells
become rearranged so as to constitute a complete girdle of powerful
cilia, behind which is an equally complete girdle of smaller cilia.

coerulea showing the mode of completion of
the prototrochal girdle. (After Wilson,
altered.)

•fi.t, primary trochoblasts (darkly shadnd) ; s.t, secondary
trochoblasts (dotted).

298

INVEKTEBRATA

CHAP.

By this time twenty-four hours have elapsed, and the embryo has
escaped from the egg-membrane and entered on its free-swimming
life as a Trochophore larva. In this larva the blastopore becomes
shifted forwards and then completely closed, but the stomodaeum

ttr

FIG. 233. — Three diagrams of sagittal sections of the early larva of PofcUit rocntleu in order
to illustrate the shift of the Mastopmv and the formation of the stomodaenm.
(After Patten.)

A, stage where the blastopore is at the vegetative pole of the egg. B, stage where both telotroch
and blastopore have been shifted forward owing to the growth of the dorsal region. C, stage wlinv
blastopore is shifted farther for wan 1 by growth of ventral region, the telotroch remaining stationary,
and in which the stomodai-um lias originated. The arrow indicates the regions of the embryo which
are undergoing rapid growth, op, apical plate ; cml, rndodermal cells ; p.tr, prototroch ; stum, stomo-
daeum ; t.tr, telotroch.

arises as an invagination of the ectoderm at the spot where the last
trace of the blastopore disappeared. The shifting is due to the
greater relative growth of the dorsal ectoderm behind the proto-
troch (Fig. 233). The endodermic cells divide and form a sac which
is the stomach ; and from the hinder end of this the intestine

IX

MOLLUSCA

299

grows out as a narrow tube. The latter comes into contact with
the ectoderm just behind a slight ventral projection carrying stiff
hairs, which now becomes apparent and which corresponds to the
telotroch of the larva of Polygordius: there the anus is formed
later. There is, in addition to the telotroch, a mid-ventral band of
very fine cilia passing forwards from the telotroch to the mouth, it
corresponds to the mid-ventral ciliated groove found in many Anne-
lid larvae, although it is not found in the larva of Polygordius.

There are, however, several points in which the larva has already
passed the stage of the
pure Trochophore larva
and entered on a post-
trochophoral stage of de-
velopment. These are as
follows : (1) In the dorsal
region, behind the proto-
troch, a thickened plate of
ectoderm cells has become
recognizable, which is
beginning to be slightly
invaginated ; this is the
rudiment of the shell
gland, the organ to which
the shell owes its origin.
(2) The mother cells of
the adult mesoderm have
proliferated, each giving
rise to a short mesodermal
band. (:5) Two slight
elevations at either side
of the mid -ventral line
have appeared, just behind
the mouth, which are the
beginnings of that char-
acteristic Molluscan organ,
the foot.

As development pro-
ceeds the life -history of

the Mollusc diverges more and more widely from that of the Annelid.
In the case of Patella the post-trochophoral stages of development
have been described by Patten (1885) ; he was able to keep the
larvae alive for a week, and has given a good account not only of
the external appearance of the larva in these stages, but also, to
some extent, of their structure, by means of sections.

Patten's account, although extremely interesting, is rather meagre,
and whets the desire for a thorough reinvestigation ; it is as follows.
As the blastopore shifts forward and finally closes near the spot where
the mouth will subsequently be formed, the two rudiments of the

stom .

m.b

FIG. 234. — Lateral view of young Trochophore larva
of Patella coentlea. (After Wilson, slightly
altered. )

ap, apical plati1 ; M, mother cell of mesoblast ; mJ>, meso-
ll'-'IInal lial"' ; S-'J> sllel" Slancl ; s'> stomach ; stum, stomo-

300

INVERTEBRATA

CHAP.

foot unite with one another in the mid-ventral line so as to form a
median protuberance. The shell gland grows greatly in extent and
depth so as to occupy the entire dorsal region behind the prototroch ;
the cells forming its floor become thin, whilst those constituting its
sides remain thick, and subsequently the imagination shallows out
and the floor becomes everted as a rounded hump. On this hump a
thin thorny membrane is secreted, which is the first rudiment of
the shell (Fig. 236). The eversion is due in large measure to the
up of the stomach. The thickened edge of the shell-

swelling

set

FIG. 235. — Ventral views of two stages in the development of the Trochophore
larva of Patella coerulca. (After Patten. )

A, stage in which the blastopore extends to the posterior pole of the embryo. B, stage in which the
blastopore is closed and the stomodaeinn is formed. Letters as in the previous figure. In addition,
I'lp, blastopore ; /, foot ; set, prominences in the pretrochal region bearing stiff setae.

gland region constitutes the rudiment of the mantle fold ; under it
appears a groove, deepest behind, and this deep spot is the rudiment
of the mantle cavity. The rounded hump on which the cap-like
shell is secreted is the visceral hump.

The larva with its projecting foot and cap-like shell is termed a
veliger; and its enlarged prototrochal girdle is called the velum.
At first the visceral hump and shell project forwards, but in
the latest stage observed by Patten they project backwards (Fig.
237). How this change was effected Patten did not observe ;
but it has been observed by Boutan (1899) in -the closely allied
genus Acmaea, and in other primitive Gastropoda, like Fissurella

IX

MOLLUSCA

301

and Haliotis, which, like Patella, are members of the division
Aspidobranchiata.

Patten made out some other interesting points in the develop-
ment of Patella. The radula sac appears as a ventral pocket-like
outgrowth of the stomodaeuni (r.s, Fig. 236). The anterior ends of
the mesodermic bands break up into loose tissue, like mesenchyme.
Some of this tissue develops into long spindle-shaped cells, which are
muscular and which are inserted at one end into the ectoderm of
the visceral hump and at the other into the sides of the stomach.

FIG. 236. — Side view of a veliger larva of Patella coerulea before torsion has taken place.

(After Patten.)

a, position of anus ; /, foot ; int., intestine ; m.f, mantle fold ; muse, retractor muscle of the shell ;
o, mouth ; r.s, radula sac ; sh, shell ; st, stomach ; stom, stomodaeum ; ttr, telotroch ; V, velum ;
v. h, visceral hump.

Others of these cells form muscles connecting the apical plate with
the sides of the oesophagus (as in Polygordius}.

The otocysts are formed quite early, whilst the foot is still
quite inconspicuous, as two elongated pits situated just behind the
mouth on either side. Later, when the foot grows out and becomes
very conspicuous, two ectodermic thickenings appear on its anterior
surface, and are interpreted as the rudiments of the pedal ganglia.

"What are most probably the rudiments of the cerebral ganglia
are shown in Fig. 239, where, at the sides of the persistent apical
organ with its powerful cilia, two ectodermic thickenings are seen.

302

INVEETEBEATA

CHAP.

The cerebral ganglia of Patella, on this supposition, would arise in the
same way as those of Polygordius, at the sides of the apical plate
(see Chap. VII).

The rudiments of the eye cups probably arise on the velar area at
the sides of the apical plate, where two groups of three or four clear
cells are seen, around which pigment is developed (o.c, Fig. 237).
Curious prominences bearing stiff setae appear on the velar area
at the sides of the apical plate. One is tempted to regard these as
the rudiments of the tentacles, but according to Patten they
disappear.

As the foot grows large the otocysts, which at first lie in front

me.

FIG. 237. — Side view of a veliger larva of Patella coerulea after torsion has taken place.

(After Patten.)

Letters as in previous figure. In addition, m.c, mantle cavity ; o.c, rudiment of eye ;
iil>, operculum ; p.g, rudiment of pedal ganglion.

of it and which have become detached from the ectoderm, move into
it. On the posterior aspect of the foot a thin operculum is developed,
which is large enough to close the aperture of the shell. The shell
itself, which was at first thin and chitinous, becomes much thicker
and calcareous, with a corrugated surface. At the latest period at
which Patten observed the prototrochal girdle or velum, it consisted
of three concentric rows of cells, a middle row of very large tall cells
carrying very powerful cilia, and an anterior and posterior circle of
cells carrying much smaller cilia.

It will be seen that a thorough investigation of the manner in
which the organs of Patella are built up has yet to be made;
Patten's description must be regarded as a first sketch. He did not

IX

MOLLUSCA

303

succeed, iu keeping his larvae alive for more than a week. Kecently,
however, the larvae of Patella vuljata have been reared through their

met

m.

ttr

Flo. 238. — Frontal section of a veliger larva of Patella coernlea in order to show the
mesodennie hands. (After Patten.)

a;), apical plate; in.li, mesodermic band ; m.ch, mesenchyme cells budded off from the front ends
of the mesodermic bunds ; at, stomach ; t.tr, telotroch ; V, velum.

FIG. 239. — Frontal section through the pretroehal region of an old veliger larva of

Patella coerulea. (After Patten.)
Lrtteis as in i>re\ ions figure, c.ij, rudiment of cerebral f?anxlioii.

entire metamorphosis, until they assume tlie adult form. This result
has been accomplished in Plymouth, using Nitschia as food. The field
is therefore open for a renewal and revision of Patten's work.

304

INVEETEBEATA

CHAP.

OTHER GASTROPODA

It has been mentioned above that the metamorphosis into the
adult form, so far as its external features are concerned, has been
worked out in Acmaea, Fissurella, and Halwtis by Boutan (1899).
Taking Acmaea as an example, since it is closely allied to Patella,
we find, according to Boutan, that as the visceral hump becomes
longer, the alimentary canal, consisting of larval stomach and
intestine, becomes bent into a U shape ; the mouth and anus being
comparatively near each other, separated only by the small foot.
Suddenly the incipient mantle-cavity, and the anus which opens into
it, which were originally situated in the middle line behind, become
twisted upwards and forwards so as to open on the neck of the

ten

muse.

en

int

h

Fio. 240. — Two views of the advanced stages of development of Acmaea rinjinea.

(After Boutan.)

A, Lateral view of veliger larva. B, Dorsal view of youu.n .{rumen just after the velum has brni cast
off. a, anus ; /, foot ; gl, glands in the mantle roof ; int, intestine ; muse, retractor muscle of shell ;
oc, eye ; up, operculum; ot, otocyst ; pst, peristome ; sh, larval shell ; ten, tentacle ; V, velum.

larva. According to Boutan this torsion, which is due to the
unequal growth of the two sides of the larva, takes place with
great rapidity, and as a result of it the apex of the visceral hump
hangs backwards (cf. Figs. 237 and 238).

The growth of the mantle edge continues to be uniform all round
its periphery, and produces an everted, conical lip to the shell, which
is termed the peristome. At the sides of the apical plate the eyes
and tentacles have made their appearance. Soon the velum is
cast off and the young mollusc sinks to the bottom. The peristome
continues to grow until it forms the adult conical shell ; finally the
visceral hump is withdrawn from the tiny cap-like larval shell and it
is cast off, and thus the adult state is attained. There is no reason-
able doubt that the later development of Patella is in all respects
similar to that of Acmaea.

IX

MOLLUSCA

305

In Fissurella the development is essentially similar; in this
genus also there is a cap-like larval shell which is eventually cast off;
but in the expanded peristoine a notch appears, due to a correspond-
ing indentation of the mantle
edge. As growth continues
this notch is pushed further
and further up towards the
apex of the adult shell,
because the indentation in
the mantle edge becomes con-
verted into a hole by the
formation of a bridge of tis-
sue across its lower end ; the
mantle edge in this way re--
acquires a smooth, rounded
margin, and then secretes, in
later periods of growth, con-
centric unbroken rings of

O

peristoine.

In Haliotis the larval shell
persists throughout life and
the notch in the mantle edge
is permanent, and as a result
a row of holes in the adult
shell is produced, since partial
unions of its edges, which
secrete bridges of shell, are
formed across its upper and
older part. In Haliotis the
growth of the peristoine is not
quite even on the two sides of
the mantle edge, and as a
consequence the embryonic
shell becomes pushed to one
side. This is the first indica-
tion of the spiral twist so
conspicuous in the shells of
most Gastropoda.

FIG. 241. — Three views of the just-metamorphosed

Acmaea virginea to show the formation of the
adult shell and the loss of the larval shell.
(After Boutau.)

A, dorsal view of stage in which larval shell is
retained as an apical knob. B, lateral view of a similar
stage. C, lateral view of stage, in which the larval shell
has been cast off. Letters as in previous figure.

EXPERIMENTAL EMBRYOLOGY OF PATELLA

We now pause to consider a question which must have presented
itself to the mind of the reader when we described in detail the
typical seriatiou of cell divisions in Polygordius : namely, are these
cell divisions important as separating materials destined to form
various organs, or are they merely a means for effecting an
approximately even distribution of nuclear material ?

No experiments have been made which will allow us to answer
VOL. i x

306

INVEKTEBEATA

CHAP.

this question in the case of Polygordius, but in the case of the
essentially similar development of Patella the question has been
answered by Wilson. Herbst has shown that if the segmenting eggs
of marine Invertebrates are deprived of their fertilization membranes
by shaking, and are then exposed to the influence of an artificial sea-
water from which calcium has been excluded, the blastomeres which
are formed by successive cleavages fail to cohere, and instead of a
Metazoon consisting of many cells, a heap of isolated cells is
produced.

This method was applied by Wilson (1904) to the study of
Patella, as follows. The eggs were allowed to segment in normal
sea-water until they had attained the 16, 32, or 64-cell stages. They
were then transferred to artificial sea- water devoid of calcium, and

FIG. 242. — Two views of the young Haliotis tuberculata to show the formation of the

adult shell. (After Boutan.)

A, stage in which the larval shell is still relatively large. B, stage in which the larval shell is
relatively very small, and in which the holes in the adult shell have appeared. [B is less magnified
than A.] Letters as in two preceding figures. In addition, H, heart; h, holes in adult shell.

when the blastomeres had separated from one another either
completely or so as to form small groups of cells, the isolated
blastomeres or groups of blastomeres were returned to normal sea-
water and allowed to develop further. The tendency to spontaneous
isolation does not, however, immediately cease when this is done,
and so, for the earliest stages, Wilson did not use artificial sea-water
to produce separation, but divided the first two blastomeres from one
another by means of a fine scalpel under a dissecting microscope.
Eveu for later stages he found it advisable not to wait till the
separation had been completely effected by the artificial sea-water,
but as soon as loosening had taken place he completed the separation
either by a scalpel or by blowiug a jet of water on the egg through a
fine pipette. When the experiment was performed on a larva which
had begun its free-swimming life, the method adopted was simply to
leave it in the artificial sea-water for twenty-four hours, without

ix MOLLUSCA 307

aiding the effect of the water either by shaking or cutting the larva
with a scalpel.

An isolated hlastomere of the 2 and 4-cell stages was found to
be exceedingly dillicult to rear ; it always segmented as if it formed
part of a complete embryo. In most cases the resulting mass of cells
flew into pieces without producing anything which could be called
a larva. In a few cases, however, this disruption did not happen,
and then there resulted a larva of diminished size and of the closed
or open type. Such larvae may be termed closed, or open dwarf
larvae respectively. By the latter term, is meant a larva in which
the half or quarter ectoderm does not cover the whole egg, by the
first term a larva in which, by secondary shiftings of the cells, the
inacroineres are entirely covered by ectoderm. In the closed type of
larva, in spite of these secondary shiftings, each cell undergoes the
fate which would have befallen it had it formed part of a perfect
egg ; thus a larva developed from a single blastomere of the 2-cell stage
produces only two groups of primary trochoblasts, and a larva from a
blastomere of the 4-cell stage only one. It is obvious that in
these closed larvae, each cell forms a larger part of the periphery of
a sphere than it would normally do ; and it must, therefore, be
subjected to a considerable strain in order to produce such an
abnormally sharp curvature, and this strain may account for the
explosive character of these dwarf larvae. These larvae, if they live,
always finally " close," and then gastrulation occurs : they always
produce an apical organ.

Much greater success attended Wilson's efforts to separate the
microrneres of the 8-cell stage. These when isolated segmented
exactly as if they still formed part of the whole egg ; at the end of
twenty-four hours they were converted into little ectodermic vesicles,
with an apical organ at one end and a group of four primary trocho-
blasts with their long powerful cilia at the other (Fig. 243, A and B).
When the entire group of the first four rnicromeres were isolated
they also segmented as if they still formed part of the entire egg ;
but they proved to be a very unstable combination, some cells always
separated, and the largest dwarf larva that was obtained represented
the products of the division of only three micronieres.

When the products of the division of the first quartette of
micromeres were isolated, similar results were obtained. Such cells
always segmented as if they formed part of the entire egg, and later
endeavoured to round themselves off and form ectodermic vesicles.
Thus, cells belonging to the group Iq1 developed into ectodermic
vesicles with an apical organ at one end and two secondary trocho-
blasts at the other ; these secondary trochoblasts being at once
distinguishable from the primary ones by the smaller size of their
cilia. Cells belonging to the group Iq2 divided into a group of four
primary trochoblasts ; cells belonging to the groups Iq21 or Iq22
divided once and produced a pair of trochoblasts ; cells of any
of the groups Iq211, Iq212, Iq2"1, or Iq222, when isolated, did not

308

INVERTEBEATA

CHAP.

divide, but acquired the long powerful cilia characteristic of a
trochoblast.

The macromeres of the 8-cell stage, i.e. IA, IB, 1C, and ID,
when isolated, usually either died or formed masses of cells which
disintegrated ; but in some few cases larvae were obtained. In all
cases a second quartette cell was formed, which divided as it
normally does, into a lozenge-shaped group of four cells ; then a third

B

FIG. 243. — Illustrating the results obtained by separating the blastomeres of the
developing egg of Patc/ln cucndea. (After Wilson.)

A, under view. B, lateral view of the larva, resulting from the development of a single isolated
micromere of the first quartette. The four primary trochoblasts are shaded. The other cells bearing
cilia in B are apical cells. C, lateral view of the larva, resulting from the development of one of the
J'uur macromeres of the S-cell stage. Two secondary trochoblasts are seen, and two feebly ciliated cells,
which are probably a portion of the mid-ventral ciliated groove. The endoderm cells are shaded. D,
lateral view of the larva, resulting from the development of one of the micromeres of tin' second
quartette. Two secondary trochoblasts are seen, and two feebly ciliated cells, probably a portion of
the mid-ventral ciliated groove. The interior of the larva contains loose cells representing the so-
called mesectoderm.

quartette cell was formed which divided into two, and a cell belonging
to the fourth quartette was also produced.

When a larva was obtained from one of these isolated macro-
meres the mass of cells belonging to the second and third quartettes
were seen to have undergone such displacement as to form a complete
ectodermic covering for the macromeres, and gastrulation had
occurred. At the one end of the embryo were two cells bearing

ix MOLLUSCA 309

powerful cilia. These were obviously the secondary trochoblasts
originating from the second quartette ; and the fact that there were
two, suggests that normally two cells are contributed to the forma-
tion of the prototroch in each quadrant by this quartette. At
the other end of the larva were two feebly ciliated cells. These
appear to be cells belonging to the third quartette which normally
form part of the ventral ciliated groove of the larva, they bear
exceedingly fine cilia (Fig. 243, C).

If one of the residual macromeres 2A, 2B, 2C, or 2D was isolated,
i.e. a macromere of the 16-cell stage, a very similar development was
obtained. Of course, only cells of the third and fourth quartette were
produced, and the formation of a complete larva was very rare. Never-
theless in a few cases this did occur. When it did occur the larva
had an internal endodermic mass of cells ; but it had no trochoblasts,
though two of its cells bore weak cilia. These latter would have
formed part of the ventral ciliated band if they had been a portion
of a whole larva.

When micromeres of the second quartette were isolated they
produced, like the micromeres of the first quartette, ovoid ecto-
dermic vesicles with one or two ciliated cells at one end. These
are the one or two secondary trochoblasts that are normally produced
from this quartette. The vesicles often have some cells in the
interior, and these cells are almost certainly the so-called mesecto-
derm or larval mesoderm, i.e. cells which sink into the blastocoele and
normally produce larval muscles. Such cells have been described in
Polygordius and in the development of other Mollusca, and they will
certainly be found to exist in the normal development of Patella
when this has been exhaustively analysed (Fig. 243, D).

Reviewing the experiments which have been described, we see
that they prove conclusively that cells from the early stages of
Patella, when isolated, give rise to nothing different from what they
would have given birth to had they remained part of the egg, and
that therefore the cleavage of the egg, from the first, separates
definite organ-forming substances. We are dealing in fact with an
egg with specialized structure like the Ctenophore egg, and one
which is more specialized in this respect than the Nernertine egg,
since the product of one of the first two, or one of the first four
blastomeres, is not a dwarf larva of half or quarter size, but a
monstrous being with only one-half or one-quarter (as the case may
be) of the larval structures. Thus, our views as to the affinities
of Mollusca with the Ctenophora, which we deduced from the appear-
ance of the early larva of Patella, are strengthened by the constitution
of the egg as revealed by these experiments.

PALUDIXA

It has been mentioned above that the formation of the in-
ternal organs has not been fully worked out in Patella ; nor

310 INVEETEBEATA CHAP.

has it been done satisfactorily in the case of any Mollusc except
Paludina.

Paludina is, like Patella, a univalve or Gastropod, but it differs
from Patella in possessing a spirally coiled shell. It is a fresh- water
form found abundantly on both sides of the Atlantic, Its peculiarity
is that the lower part of the oviduct is enlarged to form a kind of
womb within which the eggs undergo their complete development,
leaving the body of the mother only when they have attained,
externally at least, a complete likeness to the adult. If a number of
adults, then, be collected and killed in an extended condition, by the
slow addition of minute quantities of chloral or cocaine to the water
in which they are living, and if the shells be then carefully picked
away piece by piece and the oviducts slit open, the contained embryos
may be washed out by aid of a pipette into a watch glass of normal
salt solution, examined fresh, and afterwards preserved by the
corrosive sublimate and acetic acid mixture.

The egg is very minute ; it divides regularly into blastomeres of
nearly equal size, the niicrorneres being as big as the macromeres ; it
forms a regular trochophore and then a veliger; in fact it pursues
a primitive development within the oviduct, by the secretion of which
it is nourished, and it does not depend for sustenance on the yolk
contained in its own cells.

We owe to Erlanger (1891, 1892) an exhaustive account of the
development of Paludina ; and his results, so far as the later stages are
concerned, have been confirmed and extended by Miss Drummond
(1902). So far as the earliest stages are concerned, however, Tonniges
(1896) has directly contradicted Erlanger's statements; and on this
controversy a few general remarks may be made.

Erlanger's account, written before the days when cell-lineage was
studied, commences with the gastrula stage. This stage is reached-

by a process of regular invagination such as
is found in Polygordius, not by a massive
inflow of large cells as in Patella. The
blastopore, according to him, persists as the
anus, and the stomodaeum is formed in front
of it, so that the mouth is a new perforation.
The prototroch appears, as in Patella, as a
double circle of cilia carried by two rows of
cells. On the ventral side of the intestine a
median bilobed pouch is formed, which is the
, origin of the mesoderm (Fig. 245). This pouch

FIG. 244. — Vertical section of J .,

the gastrula of Paludina becomes cut on trom the gut, loses its cavity,
vivipara. (Aftur Brian- and gives rise to two irregular mesodernial

)O O

bands which extend forwards at the sides of

''A 1>o1 the gut. Each of these bands gives off a

small compact mass at its anterior end (l.n, Fig. 246), which becomes
converted into a larval kidney (Erlanger, 1894); while the rest
of the streak breaks up into an irregular mass of stellate cells

ix MOLLUSCA 311

which span the blastocoele, extending from gut to ectoderm. In
A B

coe

coe

FIG. 245. — Formation of the coelom in. Pnhnlina rirlpara. (After Erlanger.)

A, optical frontal section of embryo in the .stage when the coelom is being formed. B, sagittal
section of embryo in this stage. C, transverse section in this stage, coe, coelomic pouch ; </, gut ;
p.ti; prototroehal cells.

the hinder end of each streak
there is, however, a compact
mass which becomes hollowed
out to form a coelomic vesicle,
the rudiment of one of the
pericardial sacs. The two nieso-
dermic bands then fuse together
in the middle line behind, and
the pericardial sacs become
pressed against one another so
that their conjoined walls form
a septum (sept, Fig. 247, B).

Tonniges denies point-blank
the existence of this ventral
sac. According to him the
adult mesoderm arises as an
ectoderuial proliferation, on
each side of the middle line,
which gives rise to the

i\ 11

seen

i. 246. — Optical frontal section <>!' aii einl>ryo
of I'l/linU/iti 1-irijiiirn a little older tlian those
ivpresented in figure 245. (After Krlanger.)

I. ii, larval ki'lnry ; m.b, nn'sublaxtir baml :
p.tr, prot'it rnc'lial c-i'lls.

irregular mass of cells

Erlanger.

Now, \ve may quite

312

INVEETEBEATA

CHAP.

confidently say that, whatever may be the true state of affairs,
Tonuiges is most certainly wrong. For what he figures as the
earliest stages of the formation of the mesoderm in Paludina are
precisely similar to later stages in the development of the mesoderm
in PJti/sa, and other forms, whose cell -lineage has been worked
out in the greatest detail. In all these .cases the origin of the adult

B

l.per

*&L

^^v

r.per

FK;. 217. — Two stages in the formation of the pericardium of Pahnlimi ririjxtrn.

(After Erlauger.)

A, hurizontal section through visceral hump, of stage in which the two mesodormic band san' still
separate— a rudiment of the pericardium has appeared in each. B, horizontal srction through visceral
hump of later stage, in which the two mesodermic bands have fused in the middle line to form the septum
separating the right and left pericardial sacs, g, gut ; l.j>er, left pericardial sac ; r.per, right pericardial
sacs ; sept, septum formed by the opposed walls of the pericardial sacs ; tr, trabecula of cells crossing
right pericardial sacs.

mesoderm has been traced to the cells of the fourth quartette, which,
as in Annelida, are part of the endoderin.

The later products of the division of the mother cells of the
mesoderm, it is true, often come into such close contact with the
ectoderm that, if one had not a complete series of the earlier stages
to examine, one would believe that there was demonstrative proof
that the mesoderm was derived from the ectoderm ; and indeed this
very mistake has been made by other German workers in the case of
other Mollusca (Meisenheimer, 1898, 1901, and Harms, 1909). The

IX

MOLLUSCA

313

difficulty iu the case of Paludina is that the complete series of
earlier stages is not at all easy to obtain, since the earlier stages of
development are passed through rapidly while the later stages of
growth take much longer to accomplish. The chances are, therefore,
that in any one womb nearly all the embryos will belong to the
post-trochophoral or veliger stages ; and Erlanger himself once
told us that to find material for the adequate study of these
earlier stages would require at least two months' search. The
opportunities for coming to a decision in the matter are far fewer
than in the case of an ordinary Gastropod, whose eggs are laid by
thousands, and where every desired stage can be had in abundance.

11

rper

rk

mf

Fie. 248.— Horizontal section through the visceral hump of an older emlirvo uf

oivipara than that represented in Fij--. '247, to show the formation of the kidneys and
the heart. (After Druininond. )

II, rudiment of hrait; h<'t>, liver; hit, intestine ; /./,-, left kidney; 1. per, left pericardia! sac; /./.,
ri.^cht kidney; r.ptr, right periruidial sac; acjit, evanescent septum between the pericardia! sacs; st,
stomach.

Eiianger's account of the matter agrees in prl/i/'//i/<' with what is
known of the development of Annelida with very small eggs, like
Eupomatus (Hydro'ides), where the mesodermal cells are budded out
from the intestine. But of course the formation of a definite pouch
is a far more primitive method of development than that so far
described for any Annelid or Mollusc, and it is a somewhat strange
thing that this mode of development should be found in Paludina,
which cannot be described as a very primitive member of the class to
which it belongs.

There the matter must rest, since Erlanger has been cut olf by
an untimely death, till some other ernbryologist has the patience to
thoroughly investigate this difficult subject.

When we reach the stage of the development of the pci K ardiuni

314

INVERTEBRATA

CHAP.

:ur

per

of Paludina, agreement happily reigns among observers. The foot
appears as a mid- ventral protrusion, the shell gland as a mid-dorsal
shallow invaginatiou. Just as in the case of Patella, the shell gland
is everted aud converted into a shell-forming area covering a visceral
hump. The mantle fold aud mantle groove appear in the same way

as in Patella, and the
A torsion process takes

place apparently slowly,
as all stages in its com-
pletion are often found.
Before this happens,
however, the rudiments
of many organs appear.
To begin with, the com-
pact mass at the hinder
end of each mesodermic
band becomes hollowed
out, as we have already
seen, to form a small
pericardial vesicle (Fig.
247), and from each of
these vesicles an evagina-
tion, the rudiment of a
kidney, is found. The
two coelornic vesicles are
at first separated by a
septum, but this is soon
absorbed and a single
vesicle,the pericardium,
results (Fig. 249). This
lies ventral to the in-
testine near the posterior
end of the embryo. The
rudiment of the heart
appears as a dip in the
dorsal wall of this sac, and
in this way a bag full
of blastocoelic fluid is
formed which hangs down
into the pericardium and
constitutes the heart
with its contained blood.
The kidney on the right side becomes marked off from the
pericardium by a constriction, and this narrow communication forms
the reno-pericardial canal of the adult. On the left side the kidney
rudiment remains small and thick-walled, and is also marked off from
the pericardium by a constriction.

The ureters or external sections of the kidneys arise as

m.f

liir Ik r.ur

rrif.

FIG. 249. — Illustrating the development of the ureters of
1'nliKli mi riri/iitru and their relation to the kidneys.
(After Erlanger.)

A, cut-off visceral hump of an embryo, rather older than
that represented in Fig. 24S, viewed from below. B, horizontal
section through the visceral hump of an embryo of the same
age as that represented in A. a.p, anal papilla; lifp, liver;
l.l;, left kidney; 1. in: left ureter; m.f, mantle fold; )ier, peri-
cardial sac (the right and left pericardial sacs of the earlier
stage have fused) ; )-./,-, right kidney ; r.ur, right ureter.

ix MOLLUSC A 315

ectodermal invagiuations. They are in reality, however, only deeper
portions of the mantle groove which intervenes between the mantle
fold and the body wall (Fig.' 249).

The embryonic stomach, whose cells are gorged with albuminous
matter, has been shifted into the visceral hump, and in this way the
alimentary canal takes on a U shape. The intestine is lined by small
cubical cells, and, by an extension of cells of this description along
the mid-dorsal and mid-ventral lines to meet the stoinodeal cells, the
embryonic stomach becomes divided into two lobes which, in later
life, become converted into the two lobes of the liver. The median
portion lined by small cells forms the adult stomach, and the radula
sac arises as a ventral pocket of the stomodaeuni.

Meanwhile the rudiments of the sense organs appear. The
otocysts (ot, Fig. 250) arise as pocket-shaped imaginations of the
ectoderm at the side of the foot. The eyes arise as similar invagina-
tions of the pretrochal area (oc, Fig. 250) ; they are formed at the
bases of two conical projections which are rudiments of the tentacles
(ten, Fig. 250).

The principal ganglia of the central nervous system arise as
separate ectodermic thickenings, the commissures connecting them
being formed only afterwards. The cerebral ganglia arise later as
two thickenings of the velar region close to the eyes. The pedal
ganglia arise similarly from the post-velar region close to the
otocysts, at the sides of the foot. The pleural ganglia arise on the
sides of the body higher up and further back ; and lastly the visceral
ganglia arise from the ectoderm of the mantle cavity, that is, the
deepest and most posterior part of the mantle groove. All these
ganglia and their commissures are established before torsion begins.

Torsion now takes place, and the mantle cavity, with the opening
of the anus and the two visceral ganglia, is rotated upwards and to
the right, so that it passes along the right side in an oblique line
until it reaches its permanent position on the back of the neck.
This torsion involves the lengthening of the intestine into a
recurrent loop, and the passage of the original right visceral ganglion
upwards and to the left, where it forms the supra-intestinal
ganglion, whilst the original left one is displaced to the right side
and forms the sub-intestinal ganglion. The right ureter passes
upwards and to the left, and the left one eventually takes up a
position on the right below it (Fig. 250, B). The pericardium and
the persistent right kidney are displaced from their original position,
underneath the gut, to a lateral position in which the kidney is
above the pericardium.

When the torsion is complete the velar cells disappear and the
tentacles become long, while the foot develops its crawling surface,
and on the upper aspect of its posterior portion the operculum
appears. The gill appears as a series of outgrowths from the roof
of the mantle cavity, and the embryo then takes on the general
appearance of the adult (Fig. 251).

316

INVERTEBRATA

CHAP.

After the embryo has escaped from the womb of the mother, the
genital organs develop. According to Miss Drummond (1902), the
genital cells are budded from the pericardial wall, close to where
the original left kidney joins it, and this kidney forms the first part
of the genital duct. Coincidently with this development the peri-

rpen.

^Jen

<?j

per

FIG. 250. — Two embryos of Paludina rhijmra viewed from the right side in order to show
the origin of the sense-organs and the beginning of torsion. (After Erlanger.)

A, stage when the foot and visceral hump are both short, and the embryo is almost bilaterally
symmetrical. B, stage when foot and visceral hump have become elongated, and in which torsion has
begun. The arrow shows the direction in which torsion takes place, n, anus ; /, foot ; H, heart ; Itep,
liver ; int, intestine ; 1. n, larval kidney ; l.jier, left pericardial sac ; /. in; left ureter ; m.c, mantle cavity ;
in./, mantle fold ; or, eye; oes, oesophagus ; at,, otocyst; r.pn; right pericardial sac; r.s, radula sac;
r.-ur, right ureter ; sit, shell ; st, stomach; leu, tentacles; V, velum.

cardium is shut off from the genital rudiment. The outer and longer
portion of the genital duct is formed by the left ureter (Fig. 252).

The torsion of the visceral hump, which results in the transference
of the mantle cavity from the posterior aspect of the hump to its
anterior face, is to be carefully distinguished from the spiral twisting
of the hump, which is shown by the spirally twisted shell ; since the

IX

MOLLUSCA

317

shell may never be spirally twisted at all, as iu Acmaea, aud
presumably in Patella, and yet the torsion may reach its extreme
limit ; moreover, torsion is always complete before the spiral twisting
of the shell begins, as is well seen in the development of Paludina.
Both changes are due to the unequal growth of the two sides of the
animal ; but whereas torsion affects the whole area of the side of the
body above the insertion of the foot, the inequality of growth resulting

r.ur

hep

•H

st

Fie. 251. — Just Latched PalmUixi n'rl/xi,-</. Sec-u from the left side and viewed as a
transparent oliject. (After Erlanger.)

a.p, anal papilla; '/.;/, buecul ganglion; &/•, rudiments of the gill; c.g, cerebral ganglion : ;/"/<,
rudiment of genital organ; H, heart; hep, liver; hit, intestine; /.»/•, left ureter; HI./, mantle fold;
oc, eye; oji, opcrculuiii ; nsj'h, osphradium ; ut, otocyst ; jied, pedal nervous cords; ]>er, pericardium;
r./c, right kidney ; r.s, radula sac ; r.ur, right ureter ; »</, salivary gland ; xf. stomach ; /•./, visceral loop
of the nervous system.

in spiral twisting of the shell affects only a more dorsal region,
leaving the floor of the mantle cavity unaffected. It is accompanied
by a lengthening of the visceral hump — and this is associated by Miss
Drummond (1902) with the outgrowth of the embryonic stomach so
as to form the adult liver. The most plausible explanation of the
inequality of growth, in both torsion and twisting, is that in the
ancestral gastropod the lengthened visceral hump fell over to one
side as the animal took to crawling over uneven ground. As a

318

INVERTEBKATA

CHAP.

result the skin on oiie side would be stretched and stimulated to
while the skin on the other side would be crushed and its

grow,

growth inhibited.

H

B

H

FIG. 252. — Transverse sections through the visceral liuiiips of two embryos of Paludina
vivipara of dill'erent ages to illustrate the torsion of the organs, the development of
the genital organs and their connection with the right kidney, and the lengthening of
the visceral hump associated with an increase in length of the liver. (After Drummond.)

A, younger stage in which the gonad is beginning as a thickening of the wall of the pericardium,
and in which the left kidney is still distinct. B, older stage in which the gonad is connected with the
rudiment of the left kidney. The right kidney has passed completely to the left. Letters as in previous
figures.

Such is, in outline, the organogeny of a Mollusc; and, as
mentioned above, Erlanger's work, except in so far as concerns the
origin of the mesoderrn, has been confirmed by the most recent
workers on Mollusca.

ix MOLLUSCA 319

METHOD OF RECONSTRUCTING ORGANS FROM SERIES OF SECTIONS

A word on certain methods is here advisable. The method of
handling and making sections of minute embryos has been fully
described in Chapter II. ; but in the examination of sections, the
observer, in looking through a series, mentally synthesises the
pictures presented by successive sections, and thus forms a conception
of the organ of which they each form part. This, with a little
practice, is a comparatively easy matter when one is dealing with a
bilaterally symmetrical animal or any animal whose body can be
compared to a cylinder ; when, however, one is dealing with an animal
which is twisted in a spiral fashion, like Paludina, the mental
synthesis is a very difficult matter, and, to assist it, the following-
method of reconstruction is followed.

The usual way of applying this method is to draw outline
sketches of successive sections at a constant magnification, for example
200 diameters. If the sections are 5^ thick, i.e. y^Vo °f a millimetre,
which is a usual thickness in dealing with minute objects, then, such a
section, being magnified in all its dimensions to the same extent
as the picture that is drawn of it, would be 1 millimetre thick.
The drawings are therefore transferred to wax plates 1 millimetre
thick, and the outline of the particular organ whose course it is
desired to study is boldly drawn in a conspicuous colour. Bound
this outline the wax plate is cut away ; and the pieces of successive
plates are piled on one another in the proper order, and in this way
the solid form of the organ is reconstructed. In theory the pieces
from successive plates should fit exactly, but in practice it is found
necessary to adapt them to each other by melting the edges with a
hot scalpel.

Prof. Graham Kerr has, however, elaborated a method by means
of which practically as good results are obtained with infinitely less
labour. Instead of wax plates he used square plates of fine ground
glass of appropriate thickness. On these the outlines of successive
sections of the organs which it is desired to reconstruct are drawn
with a pencil of coloured chalk. The plates are now piled upon each
other in proper order in a square glass vessel which is filled with
cedar oil of the same refractive index as that of the glass used—
both oil and plates being, of course, specially made for the purpose.
The result of this arrangement is that the glass becomes absolutely
invisible when immersed in the cedar oil, the coloured outlines of
successive sections stand out boldly, and the solid form of the organ
is conspicuous at the first glance. One great advantage of this
method is that the materials, glass plates and cedar oil, can be used
over and over again, since the pencil outlines are easily washed off.

OTHER GASTROPODA

We shall now examine how far the developmental history which
we have described in Patella and Paludina is exemplified in the case

320 INVEETEBEATA CHAP.

of the other Gastropoda which have been studied. We find that those
primitive forms which preserve the original bilateral symmetry (the
Polyplacophora, Chiton and its allies) possess a typical Trochophore
larva, similar in all respects, so far as our knowledge goes, to that of
Patella.

The cell-lineage of Ischnochiton, as worked out by Heath (1899),
seems to be exactly similar to that of Patella, and the formation
of organs in the European Chiton polii, as described by Kowalevsky
(1883), wears an even more primitive aspect than in Paludina; for
example, the two perieardial sacs in Chiton polii are large, and occupy
most of the post-trochophoral region. A re-examination of the later
larval history of Polyplacophora by the aid of refined modern methods
would be of rare interest.

A Trochophore larva is also found in the case of such primitive
forms as Trochus, which has been worked out in great detail by
Kobert (1902), and in Acmaea, Fissurella, and Haliotis, all of which
retain two auricles in the heart and two kidneys.

In all other Gastropoda, so far as is known, the embryo becomes a
larva only when the Trochophore stage has been passed through and
the coiled shell has been formed. Since, in almost every case, the
eggs only develop after they have been laid, this involves their being
laid in capsules secreted by the oviduct of the mother. Sometimes
many eggs are contained in a capsule (Prosobranchiata generally),
sometimes only one (Opisthobranchiata and Pulmouata), and in this
latter case the capsules are very small and generally embedded in a
jelly which is difficult to get rid of. The capsules of the Proso-
branchiata are usually large, they are unprotected by jelly and
attached singly to submarine objects such as stones. It is easy
enough to detach them and slit them open, and in this way a supply
of embryos can readily be obtained.

It is interesting to see in some such cases (of. Purpuni) the
beginnings of the same process which has led to such distortions of
development as are seen in the case of Platyheluiinthes. Some of the
embryos in a capsule develop imperfectly and are swallowed by their
successful sisters, to whom they serve as pabulum.

In dealing with the egg-capsules of Pulmonata and Opisthobranchi-
ata, which are immersed in jelly, various methods are employed.
Sometimes, as in the case of the Opisthobranch Fiona, it is found
possible to use reagents (for example, picro-acetic and picro-sulplmric
acids) which will preserve the whole mass in bulk, and the jelly with
the contained egg-capsules can then even be embedded in paraffin ;
but usually it is necessary to remove both jelly and capsules.

We may give Wierzejski's method of dealing with the eggs of
Pliysa (1905) as a good example of how this can be accomplished.
The egg-capsules are dissected out of the jelly by needles, then
they are immersed for two or three minutes in a mixture of
the solution of corrosive sublimate in water and glacial acetic
acid, and the adhering jelly is then removed by the action of

ix MOLLUSCA 321

distilled water, in which it is soluble. The egg-capsule is then opened
l>y a prick with a needle, and the embryo, as it floats out, is taken up
in a pipette and put into 30 per cent spirit, which is after a time
exchanged for 50 per cent spirit, and so by degrees the embryo can
be immersed in absolute alcohol. This method is employed when it
is desired to cut sections of the embryos.

For the study of cell-lineage, however, another method is pre-
ferred. The whole mass of jelly with its contained egg-capsules is
thrown into a mixture of equal proportions of Perenyi's fluid and
water. The jelly at first turns milky but gradually becomes clear.
Then the capsules are opened by needles and the embryos float out.
They are put into 15 per cent alcohol, and then into 30 per cent for
twenty-four hours, and then gradually brought through higher grades
of alcohol into absolute alcohol. The right moment to open the
capsules must be carefully observed ; if that time be allowed to
pass the jelly turns milky again.

A method of staining with silver nitrate was also employed by
Wierzejski, and when successful it caused the outlines of the cells to
be indicated by brown lines. A -75 per cent solution is used ; in this
the capsules are allowed to stay until they are brown, then they are
opened and the embryos washed with alcohol. Wierzejski mounts
his embryos in a mixture of balsam and clove oil, which remains
sufficiently fluid to allow the embryos to be rolled about by the
motion of the coverslip. The coverslip is supported by thin pieces
of paper, or by thin pieces of glass tube drawn out to the proper
degree of tenuity. By slight modifications of this method the eggs
of all Opisthobranchiata and Pulmonata can be dealt with.

The development of a Gastropod in which the larval stage begins
at the time when shell and foot have been formed, bears the same
relation to that of Patella as the development of Nereis sustains to
that of Poli/gordius. The most important differences are the ex-
tremely early indications of the future asymmetry, and the reduction
of the prototroch. In Crepidula, which has been studied by Conklin
(1897), and in Fiona, which has been worked out by Casteel (1904),
for example, only the anterior primary trochoblasts (i.e. the de-
scendants of la2 and lb2) develop cilia, the greater part of the ciliated
band being formed from " secondary trochoblasts," which include the
tip cell 2bu and descendants of 2b12 and 2b21, and even (in Fiona} of
certain cells of the third quartette.

If this description is followed it will be seen that the velum
consists principally of two anterior lobes ; the circle is completed
in Crepidula by a band of ciliated cells which runs across the anterior
hemisphere of the larva in front of the apical cells, in Fiona by an
ill-defined ciliated area extending over the posterior part of the
front hemisphere, and in Physa not at all. When, as in many
Prosobranchs, the state of affairs is as in Crepidula, the eyes and
tentacles are excluded from the velar area, and hence the honiology
of the velum with the Annelidan prototroch has been seriously

VOL. i Y

322

INVERTEBRATA

CHAP.

questioned ; but when the structure of the embryos of Patella,
Troclius, and Chiton was elucidated, the real hornology of velum
and prototroch became apparent.

Another difference is seen in the development of the " cross."
This becomes far more conspicuous in the case of most Gastropods
than it does in Patella. The terminations of its four arms are formed
by the " tip cells " 2an, 2bn, 2cu, and 2du. The basal cells are of
course la121, lb121, Ic1-1, and Id121, while tucked away between the
four basals and the apical cells la111, etc., are the so-called "peripheral
rosettes " la112, etc., which represent the Annelidan cross, but

which do not divide more than
once in Mollusca and hence do
not attain any great development.
The basal cells of the Mollus-
can cross, on the contrary, divide
several times transversely, and
then the daughter cells in the a,
b, and c quadrants become longi-
tudinally divided into two and
even into four rows of cells (Fig.
252). In the d quadrant they
remain undivided longitudinally
for a considerable time, but also
eventually divide, filling up the
gaps between the apical and the
prototrochal cells ; the latter
usually divide only once, forming
eight "turret cells," of which
only the anterior, as we have
seen, develop cilia. These points
can be well seen in the segmenting
egg of Crepidula (Fig. 253).
The most interesting thing that has been elucidated in the
development of these more modified Gastropods is the relation of the
organs of the veliger to certain groups of cells in the cell-lineage.
Thus, in Planorbis it is found that the cerebral ganglia arise by
internal proliferation from the lateral arms of the cross, except from
their tip cells and the cells immediately adjoining these ; from the
anterior arms, except from their tip and basal cells ; and from the two
hinder arms of the Annelidan cross.

In Crepidula, Pkysa, and Fiona it is found that the mother cell
of the mesoderm, 4d, divides as usual into right and left cells, 4dr and
4d:. These then bud off two small anterior cells whose fate is to
become endodermic, while the mesodermic mother cells divide into
equal parts ; so that we have four large mesodermic mother cells, two
on each side. From each of the inner pair of mother cells a second
small cell is given off; and these, with the first two cells, form a
group of four small cells which lie close to the macromeres behind.

FIG. 253. — Apical region of an embryo of
Crepidula showing the Molluscan cross
in a late stage of development. (After
Conklin. )

The apical cells are unshaded, as are also the
primary trochoblast cells. The "peripheral
rosette " cells (Annelidan cross) are marked with
small circles. The cells of the Molluscan cross are
ruled with horizontal lines, except the derivatives
of the tip cells, which, since they belong to the
second quartette, are dotted.

ix MOLLUSCA 32

o

When the niacromeres, by further division, have formed the larval
stomach, these four cells seem to give rise to the hinder part of the
intestine. They may be termed mesendoderm. There is no doubt
at all that a similar state of affairs will be found in Patella when the
cell-lineage has been fully worked out. It is another proof that the
coelomic cells are essentially endodermic in origin.

The so-called mesectoderm or larval mesoderm, consisting of
ectodermal cells which wander inwards and are converted into the
muscles of the larval oesophagus, is derived in Mollusca generally
from the anterior quadrants (a and b) of the third quartette.

The stomodaeum in Fiona, Crepidula, and Physa arises from
2b22!! and 2b221 in front, and at the sides from cells of the third
quartette, to a certain extent, as in Polygordius. In these Mollusca,
however, these third-quartette cells succeed in excluding 2a222 and
2C222 from the sides of the stomodaeum, whilst behind it is closed
entirely by third-quartette cells. In this case 2a222 and 2c222 give
rise to lateral ridges of cells, between which and the opening of the
mouth there are' grooves filled up by third-quartette cells. In
these grooves two pits appear (Physa) which form the rudiment
of the radula sac. The ridges formed by 2a222 and 2c222 meet behind
the mouth so as to enclose the pits and the mouth in a common
atrium or outer stomodaeum ; so that eventually 2a2'22 and 2c222 do
form the outer stomodaeum.

The foot in primitive forms, such as Trochus and Patella, is at
first double ; it arises from descendants of 2d, in the region of the
ciliated groove.

The most puzzling things about Gastropod Mollusca are the
larval kidneys. These appear to be absent in Marine Proso-
branchiata, but are found both in Pulmonata such as Limnaea and in
fresh-water Prosobranchiata such as Paludina. In these forms they
consist of V-shaped tubes with the apex of the V directed forwards,
and they are formed of one huge giant cell. The internal end, i.e.
the upper limb of the V, is a solenocyte ; the lower limb opens to
the exterior not far behind the head and a long way in advance of
the opening of the permanent kidneys. At first sight one would
be strongly inclined to regard these kidneys as equivalent to the
archinephridia of Annelida. But the painstaking analysis of Wier-
zejski (1905) has conclusively proved that, in the case of Physa at
any rate, the larval kidney arises from three cells at the anterior end
of a row which is budded from the outer mesodermic teloblast on
each side ; and Erlanger (1894) found that in Paludina the larval
kidney was segmented off from the anterior tip of the coelomic
vesicle on each side. Therefore this type of kidney really belongs to
the type whicli Goodrich terms coelomiduct, and its appearance
would seem to indicate that Gastropoda originally possessed two
pairs of coelomic kidneys — a conclusion which on other grounds
may be regarded as extremely probable.

In Opisthobranchiata, on the other hand, there is found either

324

INVERTEBRATA

CHAP.

one or a pair of dark excretory vesicles situated extremely far back in
the neighbourhood of the anus. This vesicle, in Aplysia, has been
supposed by Mazzarelli (1898) to be the rudiment of the permanent
kidney, but Holmes (1900) declares that in Fiona the main part of it
is formed from a large cell which he identifies as 3cul. In Umbrella
Heymons (1893) finds a pair of these organs which arise from 3cn
and 3d11. They thus roughly correspond to the archinephridia of
Polygordius in position.

The whole uncertainty in the matter arises from the fact that
in no single species of Opisthobranchiata have we the complete
developmental history of the organ from its earliest origin in the
embryo until the larva has metamorphosed into the adult ; and

a

FIG. 254. — Embryo of Limiiaca staynalis viewed from right side as a transparent object

in order to show the larval kidney. (Alter Erlanger. )

a, anus ; c.o, external opening of the larval kidney : /, foot ; hrp, lobes of liver ; /.», .larval kidney ;
n.c, nerve collar; o, mouth; r.s, radula sac; sh, shell ; sol, solcnocyte of the larval kidney; st,
stomach.

Comparative Embryology, so long as it is based on bits and scraps
of development, is bound to be full of obscurities and apparent
contradictions.

In Marine Prosobranchiata there are frequently present two
external protuberances of ectoderm cells, situated on each side and
behind the velum. These become filled with excreta, and are
eventually cast off. When it is remembered that the archinephridia
of Polygordius owe their origin to ectoderrnal cells, it will be seen
that it is quite possible to regard these external nephridia as

homologous with them.

SOLENOGASTRES

We now pass on to consider the developmental history in other
classes of Mollusca. The Solenogastres are an extremely primitive

ix MOLLUSCA 325

and at the same time a degenerate group, in some of which the
ventral ciliated groove is retained throughout lii'e ; but they have
been shown in one case to possess a typical Trochophore larva. This
case is that of Dondersia, and the Trochophore is gradually converted
into the adult form by the elongation of the post-trochal region.

SCAPHOPODA (Dentaliuni)

The Scaphopoda, with tubular shell and mantle, are represented
by Dental ium and a few closely allied genera. The development of
Dentalium has been worked out by Wilson (1904). It is practically
of world-wide distribution, being found in muddy bottoms. Wilson
found the eggs of the Mediterranean species ripe in June, and he
gives the following description of them. They are yolky and deeply
coloured by pigment which varies in tint from olive-green to
brownish-red. When dehisced from the ovary the egg is almost as
flattened as a biscuit, though one side is more flattened than the
other, and this side is proved subsequently to be the vegetative pole.
In the centre of each flattened surface is a white non-pigmented
area.

After remaining in sea-water for from twenty to thirty minutes the
egg becomes spherical and bursts its ovarian membrane or chorion.
A jelly-like layer which surrounds the egg then swells up, and the
egg now looks like a sphere with white poles and a broad ring of
pigment. But when the egg is fixed in picro-acetic and cut into
sections, the two poles are seen to be widely different. At the
vegetative pole there is a dense mass of cytoplasm, devoid of yolk,
which is continuous with a thin layer of clear cytoplasm surround-
ing the egg. This mass of cytoplasm also extends upwards through
the egg to the germinal vesicle or nucleus, which is situated near
the animal pole and surrounds it. At the animal pole there is a
minute disc of cytoplasm free from yolk, which is far too small to
account for the large white area seen in the living egg in this region.
This latter must owe its appearance therefore to the presence of yolk
granules of white colour.

As the egg lies in sea- water the cytoplasm of the animal pole
slowly increases in amount, seemingly by a radial inflow from sur-
rounding regions. The wall of the nucleus now breaks down and
the first polar spindle is formed. Things are now at a standstill
until the egg is fertilized, when the two polar bodies are formed one
after the other. The spermatozoon enters at the vegetative pole.
From this pole a pillar of granular cytoplasm extends upwards and
becomes temporarily confluent with the cytoplasmic area at the
upper pole. This pillar is in large measure produced by the material
which was contained in the nucleus of the unripe egg, and which was
extruded when the nuclear wall broke down.

The first cleavage occurs half an hour after fertilization, and is
vertical. At the same time the lower white pole of the egg is cut off

32G

INVEETEBKATA

CHAP.

from the rest by a horizontal constriction. Sections show two things
—first, that this lower sphere contains, besides the vegetative cyto-
plasm, a certain amount of yolk ; and secondly, that it remains in
connection with one of the two spheres produced by the vertical cleav-
age, by means of a thin pedicle never completely severed. As the
cleavage of the two blastorneres from one another becomes complete,
the lower sphere coalesces with one of the two upper spheres, and the
blastomere so formed is shown afterwards to be CD. The lower
sphere has been somewhat inappropriately named the yolk lobe, for

u-.w.s

FIG. 255. — Vertical sections of the eggs of Dentalium before and after fertilization iu
order to show the flow of cytoplasmic substances. (After Wilson.)

A, before fertilization — after extrusion from the oviduct. B, after fertilization — formation of the
first polar spindle. C, division into two blastomeres— extrusion of the first polar lobe, g.s, germinal
spot, i.e. nucleolus ; g.v, germinal vesicle; /.«.'.»•, lower white substance; n, the first two daughter
nuclei separating from each other ; y1, first polar lobe ; u.w.s, upper white substance.

which Wilson substitutes the name polar lobe, and its fusion with
one of the two blastomeres is known as the retraction of the
polar lobe.

When the next cleavage occurs, AB of course divides into A and
B, and the polar lobe is again constricted from CD, but at the con-
clusion of the cleavage it fuses with D, which is thus rendered by
far the biggest of the first four blastomeres. A and C, moreover, as
usual, meet in an upper cross furrow. Each of the four cells contains
a portion of the white area which was situated at the animal pole of
the egg, but only D has the white material of the vegetative pole.

MOLLUSCA

327

At the next cleavage the first quartette of micromeres are given
off. These consist entirely of the white material, though some of this
still remains in the macromeres. The polar lobe is again constricted
off from I), but it is much smaller than before and the constricting
furrow does not extend so deeply. When the cleavage is complete
the polar lobe again fuses with ID.

Before the next cleavage occurs the white material derived from
the animal pole, part of which was left in each macromere, increases

FIG. 2;"6. — Stages in the cleavage of the egg of DcntdUnm. (After Wilson.)

A, completion of the lirst cleavage. B, beginning of the second cleavage, seen from the skle. C, the
second cleavage in its most intense period, seen obliquely from above and the side, j.i, the first polar
lobe ; p%, the second polar lobe ; }>.b, polar bodies.

in amount, moves over to the right side of each cell, and extends
somewhat down the side. In ID this also occurs, but in this cell the
white material from the animal pole is joined by the white material
from the vegetative pole, which moves over and fuses with it. Of the
second quartette of micromeres 2d is formed lirst, and it is composed
of the white material derived from both poles, whereas 2a, 2b, and 2c,
which are formed soon afterwards and likewise consist of white
material, have received only white material which was originally at
the animal pole of the egg. At the same time the first-quartette
cells divide into the trochoblasts (lq-) and the upper cells, the latter

328

INVERTEBKATA

CHAP.

being slightl}7 larger. The third quartette is formed as usual at the
next cleavage ; 3d is larger than its sisters, and entirely composed of
white material.

After this cleavage gastrulation begins by the macromeres passing
bodily into the blastocoele, just as in Patella. Of the fourth quartette
4d alone was clearly observed ; it is smaller than 3d and very much
smaller than 2d, and is pure white.

As in Patella, cilia are developed about ten hours after fertilization,

2c

B

FIG. 257. — Further stages in the cleavage of the egg of Deiitalium. (After Wilson.)

A, beginning of third cleavage (8-blastomere stage), seen from the lower pole. B, the formation of
the second quartette of micromeres, seen from the lower pole. The greater part of the substance which
formed the polar lobes passes into 2d. C, the formation of the third quartette of micromeres, seen
from the lower pole. D, the division of the inacromere which gives rise to the mother cell of the mesn-
clerni. p'\ third polar lobe.

and in twenty-four hours well-developed Trochophore larvae are set free.
These are remarkable for their very broad prototroch, which consists
of three complete circles of large cells with cilia. The pre-trochal
region is short and conical ; it is covered all over with short cilia, and
it bears at its apex an apical plate with a long tuft of motionless
but flexible cilia. The post-trochal region is also short and conical,
and at its posterior end there is a telotroch consisting of a tuft of
short rigid hairs.

The stomodaeum has not yet opened into the gut. This latter
consists of a sac-like stomach and a short blind intestine ; the anus

IX

MOLLUSCA

329

is not yet formed. At the sides of the intestine are seen two short
mesodermal bands. In the pre trochal region two masses of cells
are seen lying to the right and
left. These are proliferated from
the ectoderm, and are almost
certainly the beginnings of
the cerebral ganglia. Very
?oon after the beginning of

slom

ap

mes

.ir

ttr

larval life the rudiment of

the shell gland can be made

out, and the everted edge of

this already foreshadows the

future mantle fold, which is

at first double, like that of a

Pelecypod.

During the course of the

next day the larva sinks to

the bottom ; the pre-trochal or

velar region becomes relatively

smaller whilst the post- trochal

region grows very much in

length, and then the velar

region becomes finally com-
pletely invaginated, and in

this way the larva attains the

stage of a veliger.

By the end of the second day not only is the shell gland

everted but a delicate hyaline
shell has been formed, and into
this the diminished prototroch
or velum can be withdrawn.
The foot has now made its
appearance as a median ridge.
At the end of the third day the
foot has become large, protrusible,
and bilobed at its free end ; and
the mantle lobes have partially
united beneath the aninnl. By
the fifth day the prototroch has
disappeared and the otocysts
and pedal ganglia can clearly

FIG. 259.— TraiLsverse section of the Trocho- ue seen • the metamorphosis may

FIG. 258. — The Trochophore larva of Jtt'it-
talium — twenty-six hours after fertilization.
(After Wilson.)

a.ji, apical plate ; mes, mesoderm ; ji.tr, prototroch ;
st, stomach ; stom, stoniodaeum ; t.tr, telotroch.

mes

pliore larva of Dentalium in the region
of the prototroch. (After Wilson.)

Letters as in previous figure.

now be said to be complete.
It is worthy of note that the
northern species of Dentalium,
which was studied by Lacaze-Duthiers, took twenty-five days to

reach the same stage.

330

INVERTEBRATA

CHAP.

EXPERIMENTAL EMBRYOLOGY OF DENTALIUM

This peculiar development . offers abundant opportunity for
experiment, as Wilson was not slow to perceive. Some of these
experiments were quite similar to those which he performed on
Patella, and led to similar results ; but the most interesting results
were those obtained by removing the polar lobe, which can be
readily done by means of a fine scalpel. When this is done at the
time of the first cleavage the embryo continues to develop, but all
the cells at the second cleavage are equal in size and possess no
lower white area, and no polar lobe is subsequently formed.

At the subsequent cleavages the micromeres given off in the
D quadrant are precisely similar in size to their sisters, and the

B

-f

mf.

tlr

tlr

FKJ. 260. — Veliger larvae of Dentalimn. (After Wilson.)

A, Veliger larva, thirty-two hours old. B, Veliger larva, three days old. Letters as in previous figure.
In addition, /, foot ; tnf, mantle fold ; x/i, shell ; V, velum.

embryo becomes a larva with a normal prototroch and a conical
pre-trochal region ; but there is no projecting post-trochal region, the
posterior surface of the larva being almost flat. The pre-trochal
region is covered, as normally, with fine cilia, but the apical tuft is
absent, and so is the thickened apical plate which is present in
normal larvae. On the other hand, the lateral ingrowths of ectoderm,
which we suppose to represent the cerebral ganglia, are present.

Such larvae live four days and then disintegrate. Occasionally
a post-trochal protuberance appears to be formed, but when this is
examined by sections it is seen to be a plug of solid endoderm pro-
jecting through the open blastopore. No mesodermal bands are ever

MOLLUSCA

331

seen. The conclusion is therefore inevitable that the first polar lobe
contains the material necessary not only for the formation of the
whole post-trochal region, but also for the formation of the apical
plate. It must also contain the material necessary for the formation
of the niesoderrnic bands.

This conclusion is confirmed by separation of the first two blasto-
meres ; both of these, when isolated, continue to segment as if they

B

Ir

FIG. 261. — -Larvae resulting from the development of eggs of Dentalium from which the
polar lobe has been removed. (After Wilson.)

A, larva, twenty-four hours old, developed from egg from which the first polar lobe has been re-
moved. B, Larva, twenty-four hours old, developed from egg from which the second polar lobe had
been removed. Letters as in Fig. 258.

formed part of a whole egg, but both subsequently give rise to larvae
which swim about, though they possess a confused irregular proto-
troch. The larva derived from AB, however, in its general structure,
resembles the larva developed from a whole egg from which the first
polar lobe has been cut off, because
it has neither apical plate nor post-
trochal region. The larva derived
from CD, on the other hand, which
carries the polar lobe, though it is
asymmetrical and has too small a
pre-trochal region, has too large a
post-trochal one and possesses a
well-defined apical plate.

If the egg be allowed to reach
the 4-cell stage, and if the polar

lobe that is then protruded, that is PlG. 262._Vertieal section of a larva of

the second one, be removed, a larva

is produced in most respects similar

to the one which arises from an egg

from which the first polar lobe is

removed; it possesses neither meso-

dermic bands nor post-trochal region, but it possesses an apical plate

and the characteristic apical tuft of cilia. Therefore the second polar

end

Dentalium developed from egg from
which the first polar lolie had been
removed, to show the absence of
mesoderm. (After Wilson.)
end, protruding plug <>f Hiidndrrni.

332 INVERTEBRATA CHAP.

lobe does not contain the specific organ-forming material for the apical
plate ; in the interval between the formation of the first and second
polar lobes it has been distributed to a different region of the egg.

Where that region is it is not difficult to determine. If the
micromeres of the first quartette be separated from each other by
allowing the. embryo to develop in artificial sea-water devoid of
calcium, then each micromere will develop into a closed ectodermic
vesicle ; but only the micromere Id develops an apical plate, and the
apical " stuff " is therefore transferred to this micromere. Now, in
Patella the apical plate is formed in larvae developed from each of
the four micromeres of the first quartette ; we have therefore in the
development of Dentalium a case of specialization, similar to that
which we often meet with in eggs with spiral cleavage, in which
one member of a quartette does the work normally undertaken by all
the sisters in other species. A case of this kind was met with in
the first case of spiral cleavage which was studied, namely, in the
development of Phinocera as compared with that of other Polyclade
Platyhelminthes.

These remarkable experiments of Wilson establish in the most
incontrovertible manner the existence of specialized organ-forming
substances in the egg of Dentalium. It is but fair to add that the
first experiments of this kind were made by Crampton (1896) on the
egg of the Gastropod Ilyanassa, where a similar polar lobe is found.

PELECYPODA — Dreissensia

We must now consider the development of that great group of
Mollusca familiarly known as bivalves and scientifically as Pelecy-
poda or Lamellibranchiata. The most complete and satisfactory
study of the development of any form belonging to this group is that
by Meisenheimer (1901) on the life-history of Dreissensia polt/morpha.
This type we may therefore select for more special study.

Dreissensia. is a genus fo-und in brackish and fresh water both in
England and on the continents of Europe and America. In form it
closely resembles the marine genus Mi/tilus, the common mussel, to
which it is regarded by many authorities as nearly allied, and from
which it differs in having the two mantle lobes firmly united for a
part of their length in the mid-ventral line, and in having the
posterior opening prolonged into two separate tubular siphons. It
is interesting from the fact that, though a fresh-water species, it retains
a long larval development of very primitive facies, whereas most fresh-
water species have a shortened, modified, and mainly embryonic develop-
ment. Dreissensia is clearly a recent immigrant into fresh water.

Meisenheimer obtained his material from one of the small fresh-
water lakes of Germany (the Ploner See). The eggs of Dreissensia
polymorpha are laid in June, and are cast forth from the mother in
masses, bound together with a slight amount of slime which is easily
washed away. The eggs have no chorion of any kind, and hence are

ix MOLLUSCA 333

quite easily preserved. For the earlier stages corrosive sublimate
and picro-sulphuric acid were the reagents used, but for the later
stages and for the free-swimming larvae Hermann's mixture of

o o

osmium tetroxide, platinum chloride, and acetic acids gave the
best results. It was necessary to paralyse the larvae by cautiously
adding cocaine to the water in which they lived, before attempting to
preserve them, otherwise they contracted themselves into shapeless
lumps in which the natural relationship of the various organs
could not be made out. The larval stages swarmed in the
lake and were captured by using a fine-meshed Plankton net, so
that the difficulties connected with artificial rearing were entirely
avoided.

A striking feature of the early development of Dreissensia is the
intermittent appearance of the blastocoele. This cavity is large
and well developed in the 2-cell stage (Fig. 263) ; it subsequently
disappears, but reappears in later stages,
such as the 8-cell and 16-cell stages.
Meisenheimer supposes that the blasto-
coele serves as a reservoir of excreta
which are periodically voided.

The egg divides into the usual four
macromeres A, B, C, and D, but of
these ILJS so much larger than the rest
that the remaining three appear much
like micromeres budded from one large FIG. 263.— Longitudinal section of
macromere. This state of affairs is the 2-cell stage of /h-ri.w/isia
worth bearing in mind in view of the poiymorpha to show the biasto-

... i-ii coele. (After Meisenheimer. )

extraordinary statements which have 6Uj blastocoele ; ™, nucleus,
been made about the development of

other Pelecypoda. When the first quartette of micromeres is formed,
Id appears first and is the largest, though the disparity in size
between it and its sisters, la, Ib, and Ic, which appear subsequently,
is not great. But at the next cleavage, when these micromeres divide,
each into two daughters of equal size, and when the second quartette
of micromeres is formed, one of these latter, 2d, is relatively enormous
in size ; it overshadows not only all the micromeres belonging to the
first and second quartettes but its own sister macromere, 2D. This
huge " micromere " corresponds to the one which Wilson, in the
development of Nereis, has termed the first somatoblast, from which
most if not all the ectoderm covering the body of the adult worm is
derived.

From the first somatoblast of Dreissensia, termed by Meisenheimer
X, is derived the shell-gland, and we have strong reason to suggest,
although this is not quite proved, the foot ; it has, however, been
proved by Lillie (1895) in the case of Unio. The first somatoblast
now gives off a cell below and to the right. This cell is of course 2d- :
it is denominated by Meisenheimer xa, since he calls the parent
somatoblast X. At the next cleavage all the daughters of the first

334

INVEETEBEATA

CHAP.

quartette divide again, so that we get four concentric circles of cells,
Iq11, lq12, lq21, and lq22.

The third quartette of micromeres now begins to be formed, 3d
being formed before its sisters. X gives rise to a small cell on the left,
the proper title of which is 2d12, but which is called by Meisenheimer
x2. The somatoblast has thus acquired at its lower border a wreath of
three cells, xx, 3d, and x2. Of the second quartette of micromeres, which
should have divided when the third quartette was being formed, only

M

FIG. 264. — Stages iu the cleavage of the egg of hreissennin

(After Meisenheimer.)

A, upper hemisphere of egg in the 16-cell stage. B, upper hemisphere of egg just passing into the
54-cell stage. Tlie formation of the apical cells is seen. C, egg seen from the vegetative pole in the
8-cell stage at the moment when 2d is being formed. D, Posterior view of egg in a somewhat later
stage than that shown in B, to show the primary mesoderin cells and some of the products of the
division of X. M, primary mesoderm cell ; ji.1i, polar body.

one (2d = x) has as yet divided. Another member of this
quartette now divides, i.e. 2c ; whilst 2d2 divides into 2d21 and 2d22
—or, according to another notation, x: gives xn and x10.

It is quite clear therefore that in Dreissensia, unlike Patella, the
radial symmetry of the spiral type of cleavage is very early interfered
with, and that the prospective importance of the organs derived from
2d is reflected back into a very early stage of ontogeny; this is testified
to by the precocious divisions and development of the cells derived
from this blastomere.

The remaining members of the third quartette of ectoderm cells,

ix MOLLUSCA :j;;5

3a, 3b, and 3c, are now budded off' from their respective macromeres.
Only after this has happened do the anterior cells of the second
quartette, viz. 2a and 2b, divide into 2ax and 2a2, 2bJ and 2b2, respec-
tively ; whilst the sornatoblast X buds off from its upper border a
small cell x3.

All the cells of the first quartette now undergo renewed cleavage,
so that we have eight circles of cells, viz. lqm, lq112, lq121, lq122, lq211,
lq212, lq221, and lq222. In these divisions the members of each circle
belonging to the D quadrant divide before their sisters. We have
thus in J)reissensia the same typical divisions of the cells of the first
quartette which are found in Patella and Polygordius ; but
Meisenheimer does not refer to or figure any conspicuous cross-like
arrangement of any of these cells ; on the contrary, he seems to imply
that they continue to have a concentric arrangement.

At the lower pole of the egg a single representative of the fourth
quartette is now given off. This is 4d, which Meisenheimer calls the
" second somatoblast " ; but it is of course homologous with the
mother cell of the niesoderm in both Polygordius and Patella. At first
the mother cell of the mesoderm, which we may designate as M, touches
the second somatoblast ; but the latter gives off a cell towards the
vegetative pole which Meisenheimer calls x4, and this, along with xx
and x2, completely separates X and M (Fig. 264, D).

After a few more divisions in the cells of the first quartette, the
first unmistakable traces of bilateral symmetry make their appear-
ance by the division of both X and M into right and left halves.
Then from each half of X a small cell, x5, is budded off posteriorly,
and the arrangement of the derivatives of the first somatoblast is as

shown below, viz. :

X - a?3 - X :

X2 ~ X5 ~ X4~ X5 ~ XT

Each half of M also buds oft' a small cell, and then, by repeated
transverse divisions, a longitudinal plate of large cells which is tlnv
rudiment of the shell gland is developed out of the two halves of X.

Following the stage which we have just described, the process of
gastrulation begins. The residual macromeres 4A, 4B, 40, and 41)
sink inwards towards the blastocoele. The small cells given off from
the mother cells of the niesoderm sink in with them and go to build up
the wall of the mid-gut. The mother cells should therefore be termed
mesendoderm, not true mesoderm ; they themselves lie posterior to
the lip of the blastopore, and are partly invaginated with the endoclerm
in the process of gastrulation. By repeated division they give rise
later (just as in Paludina} to a loose meseuchymatous mesoderm, out of
which the connective tissue and muscles of the adult bivalve are formed.

The invagination of the mid-gut cells proceeds at first very slowly,
because their progress is impeded by the much more rapid ;ind
conspicuous invagination of the cells forming the shell gland. This
latter deep invaginatiou lasts only a short time. Soon the cells
forming the shell gland are again everted and form, as in Patella, a

oo

6

INVERTEBKATA

CHAP.

saddle-shaped plate with thickened edge, on the dorsal surface of the
larva. On this plate a thin horny secretion, the first rudiment
of the shell, appears. As the process of eversiou takes place the in-
vagination of the endoderni goes on rapidly, and soon a sac is formed
whose wall is composed of large columnar cells, and which opens to
the exterior by a constricted opening, the blastopore (Fig. 265).

B

stom

FIG. 265. — Sagittal sections of embryos of Dreissensia polymorpha, showing the process
of gastrulation and the formation of the shell gland. (After Meisenheimer. )

A, stage in which the endoderni and the shell gland are both beginning to be invaginated. B, stage
in which the invagination of the shell gland has reached its maximum. C, stagr in which the blasto-
pore is closed and the shell gland is beginning to be evaginated. D, stage in which the shell inland is
completely evaginated and the stomodaeum is beginning to be formed. o.;>, apical plate ; !>!, blastopore ;
cm/, endoderni ; h>p, cells which will eventually form the liver ; M, primary mesoderm cell ; ji.tr, proto-
troch ; s.g, shell gland ; stum, stomodaeum.

The blastopore becomes shifted forwards and finally closed in the
position where the mouth afterwards opens. This forward shift seems to
be largely due to the growth of the band of small cells, xl - xfl, derived
from X, which separated originally X and M on the posterior surface
of the embryo. This band thus comes to occupy the region immedi-
ately behind the mouth ; and as the fuot is Inter developed in this
region, it probably owes its origin to these cells. When the
blastopore has been completely closed, the stomodaeum originates as

IX

MOLLUSCA

P.37

an ectodermic iuvagination just where the last trace of the blastopore
was situated.

The wall of the mid-gut, after the blastopore has become closed,
undergoes a characteristic differentiation. The cells forming its
anterior wall acquire large clear nuclei with conspicuous nucleoli,
whilst those forming the lateral and posterior walls retain small
deeply staining nuclei. Soon the peculiar cells of the anterior wall
become confined to two slight outpouchings of the wall of the
stomach, to the right and the left of the mid-ventral line. These
pouches of the larval stomach will eventually give rise to the adult
liver. From the posterior wall of the stomach is developed the
intestine, and this grows
backwards and becomes
attached to the ectoderm
behind the mouth. Here a
very shallow in vagina tion is
formed, the proctodaeum ;
arid at a slightly later stage,
by the union of the procto-
daeum and intestine, the anus
becomes opened. In front
of the anus is formed the
teloroch, consisting of a
couple of cells carrying stiff
hairs.

So far we have not men-
tioned the prototroch and
the apical plate. Both
these structures appear about
the time when the shell
gland is everted ; the proto-
troch is in the form of a
girdle of cells carrying
powerful cilia, and the apical

stom

llr

FIG. 266. — Young Trocliopliore larva of Dreis-
scnsia polymorphic, seeii from the ventral side.
(After Meisenheimer.)

Letters as in previous figure. In addition, t.tr, telotroch.

plate in the form of a group
of cells at the animal pole bearing a wisp of long stiff cilia. The cell-
lineage of the cells forming these organs Meisenheimer was not able
to determine, but there is no reason to doubt that it is, in the main,
the same as in Patella. The prototrochal cells develop vacuoles in
their interior, as is the case with the prototrochal cells of Polyyordius.

Lastly, situated just behind the spot where the anus will develop,
there is a group of small cells which Meisenheimer believes to be of
ectodermal origin, which will give rise, at a later period, to the
coelomic sacs and to their derivatives, the kidneys and genital
organs. This cell-group occupies precisely the same place as does
the first rudiment of the pericardium in Paludina, and as do the
mother cells of the mesoderni in an earlier stage of development in
Dreissensia. When this stnge of development has been attained, the

VOL. i z

338

INVEKTEBKATA

CHAP.

embryo bursts the egg-membrane and enters on its free-swimming
life as a Trochophore larva (Fig 266).

In Physa, as we have already seen, Wierzejski has traced the
pericardium back to its origin in the derivatives of the mother

mesoderm cells, through

unbroken

For these

Meisenheimer's

origin

int-

an

series of stages.
reasons we reject
view of the
of these cells, and
believe that they are derived
from the mother mesoderm
cells after the latter have
given off the mesenchymatoiis
tissue alluded to above. This
p.tr view would bring the develop-
ment of Pelecypoda into
harmony with that of other
Mollusca, and should be
definitely tested.

The Trochophore larva soon

FIG. 267.-Sagittal section through a young Pass.es int° the Condition of a

,•/>/!«. Vellger larva. This change

takes place by the enlargement

Letters as in Figs. 265 and 260. In addition, cue, of the prototl'Och into the

velum an(l |)y t{ie oTO\vth of
Ve UJ „

the bivalve shell. Behind the
prototroch several rows of

•stom

coe

ttr

Trochophore larva of Dreissensia

(After Meisenheimer.)

group of cells from which the coelom (pericardium)
later develops; int, intestine; sh, primary shell (the

hinge).

FIG. 268. — Transverse section of the ventral portion of a young Veliger larva of l)n-i.wnxi«
polymorpha to show the origin of the mantle-groove and of the j><'</,/l <nni<jliti.
(After Mei.senheimer. )

m.c, mantle-groove ; p.<j, thickenings of ectoderm which will sive rise to the pedal i;an.u'lia ; xli, shell.

large cells are differentiated ; they are covered with numerous fine
cilia and reinforce the action of the prototrochal girdle ; this enlarged

x MOLLUSCA 339

structure is now known as the velum. These additional cells remind
us of some of the " secondary trochoblasts " of Patella.

The shell of the Trochophore is merely a thin horny cuticle
secreted by the cells of the everted shell gland. This cuticle adheres
closely to the ectoderm in the mid-dorsal line, and the ectoderm cells
here become columnar ; this region constitutes the hinge of the adult
shell. The cuticle adheres loosely towards the sides, but at the edges
of the shell gland a renewed deposition of cuticle takes place in two
small circular areas which rapidly extend in dimensions, and in this
way the valves of the bivalve shell are laid down. Not merely horny,
but also calcareous material is secreted by these shell-forming areas.

coe

a.

FIG. 269. — -Young Veliger larva of Dreissensia, polymorpha, seen from the side.

(After Meisenheimer.)

it, aims ; utlil.a, adductor muscle ; a.p, apical plate (afterwards becomes the anterior adductor muscle) ;
coe, rudiment of coelom ; c./i, cerebral pit ; tr.x, crystalline sac ; hep, lobes of liver ; in/, intestine ; l.-n,
larval kidney; m.ti; metutrocli ; <>, mouth ; p.it, pedal ganglion; r.d, dorsal retractor muscle; r.m,
middle retractor muscle ; /•. <•, ventral retractor muscle ; xli, shell; t.fr, telotrocli ; r.g, visceral ganglion ;
V, velum.

The larva now changes its shape and instead of being cylindrical
becomes more or less laterally compressed. As the newly formed shell
valves extend towards the mid- ventral line, the mantle-cavity appears
as two longitudinal invaginations on the ventral surface (Fig. 268).
By the appearance of these grooves the edges of the area formed from
the everted shell gland are changed into right and left mantle-lobes.
The valves of the shell have a characteristic shape which appears to
be practically universal amongst the veliger larvae of Pelecypoda.
The hinge-line is straight and horizontal and the lower margin of
the valve is curved, so that the shape of the whole may be described as
semicircular (Figs. 269, 271).

Behind the mouth, which is situated on a projecting oral cone, is

340

INVEETEBEATA

CHAP.

a post-oral tuft of cilia, the sole representative of the metatroch of
Annelida. The oesophagus is ciliated, and small organisms are whisked
into the stomach. The modification of the anterior wall of the stomach
into the liver-pouches has already been mentioned. From its posterior
ventral wall a short pouch grows out on the left side, whose cells
secrete rod-like excrescences. This is the rudiment of the crystal-
line sac which secretes the crystalline style (Figs. 269, 270).

A larval kidney, consisting of a straight tube opening at the

cr.s.

FIG. 270. — Young Veliger larva of Dreissensia polymorpha, seen from the ventral surface.

(After Meisenheimer.)

Letters as in previous figure. In addition, m.c, mantle-cavity.

side of what is afterwards the foot, and terminating internally in a
solenocyte situated near the liver-pouch, makes its appearance at
the same time as the shell and disappears as the foot grows out.
Meisenheimer derives it from an ingrowth of the ectoderm, but he
has no convincing evidence to prove this. We think it more probable
that it arises, as Wierzejski (1905) has proved that it arises in Pliysa,
from cells budded off from the" mother mesoderm cells.

Three sets of powerfully developed muscles are formed, consist-
ing of spindle-shaped cells which arise from the proliferation of the
mesoderm cells. All three are inserted into the cuticle of the hinge

IX

MOLLUSCA

341

in the posterior dorsal region, and all pass forwards and slant down-
wards. The uppermost of these is the dorsal retractor, the fibres
of which pass forwards and diverge to the right and left and are
inserted into the upper parts of the velum ; below it lies the median
retractor, which sends fibres to the lateral and ventral parts of the
velum ; whilst below this again lies the ventral retractor, which is
inserted into the anterior portions of the right and left mantle-lobes.
All these muscles are of a transitory character and disappear when

P-9

FIG. 271. — Older Veliger larva of Dreissensia polymorpha, seen from the side. This stage
is the one which immediately precedes the metamorphosis. (After Meisenheimer. )

Letters as in two previous figures. In addition, mhl.a, anterior adductor muscle ; add.fi, posterior
adductor muscle ; In-, rudiments of gill-papillae ; '<i/«, liyssus gland ; /.•, rudiment of kidney ; nt, otocyst ;
per, rudiment of pericardium.

the free-swimming life is given up ; but the anterior adductor
muscle, passing from one valve of the shell to the other, is already
formed at this stage, and it persists into the adult.

The three pairs of ganglia characteristic of Mollusca make their
appearance at this stage. Of these the cerebral ganglia owe their
origin to a bilobed pit, termed the cerebral pit, situated within the
velar area in front of and below the ciliated apical plate. This pit
evidently corresponds to the two lateral thickenings of the velar area
in Patella. From the bottom of this pit a bilobed mass of cells is

342 INVERTEBRATA CHAP.

separated off, which differentiates itself into two lateral masses of nerve
cells with fibres between them (c.p, Figs. 269, 270, and 271). The
pedal and visceral ganglia arise as two pairs of thickenings of the
ectoderm of the ventral surface, one pair being situated close behind
the other (Fig. 269). In addition a pair of pleural ganglia make
their appearance as a small pair of thickenings of the lateral ectoderm
of the body, half-way between the rudiments of the cerebral and pedal
ganglia ; in later life they fuse with the cerebral ganglia (Fig. 274).

The otocysts arise as small spherical imaginations of ectoderm, at
the apex of the mantle-groove. They are situated in the region which
is afterwards converted into the foot.

Towards the end of larval life the foot makes its appearance. It

..a

per

I f It > • *. I » V /

I

FIG. 272. — Transverse section through the dorsal region of old Veliger of Dreissensia poly-
•inorjihtt in order to show the differentiation of the pericardium and the kidneys.
(After Meisenheimer. )

coe, first rudiment of pericanlial cavity ; //, heart ; Jt.n, hin.^e area of shell ; int, intestine ; l.k, left
kidney ; per, ring of cells which gives rise to pericardium ; r./,1, ri.n'ht kidney ; sli, shell.

is defined by two transverse furrows, an anterior and a posterior, the
latter cutting in deeply between the pedal and the visceral ganglia
and separating them from one another. On the posterior aspect of
the foot a deep invagination occurs which is lined by columnar cells.
This is the rudiment of the byssus gland, which secretes the cords of
horny material by means of which the adult Dreissensia anchors itself.
The forepart of the foot grows into a finger-like process covered with
minute cilia,, and the primitive kidney disappears.

The intestine becomes bent into a slight loop ; it runs upwards
from the stomach and bends downwards and forwards to reach the
anus.

The posterior adductor muscle is formed by a modification of
some of the spindle-shaped cells of the mesenchyme, and so also is the
retractor of the foot. This retractor muscle is a mass of fibres
which project downwards from the posterior part of the mid-dorsal

IX

MOLLUSCA

343

region

c

P

surrounding the end of the intestine and extend into the
hinder region of the foot.

The first rudiments of the gills appear as a row of short, knob-like,
ciliated protrusions from the roof of the mantle-groove, on each side
and parallel with the pos-
terior surface of the foot
(br, Fig. 271). The coelomic
rudiment becomes divided
into a rounded mass of cells
on each side of the intestine,
which are the rudiments of
one kidney, and into an
arch of cells above the gut
connecting these two rudi-
ments. In the very last
stage before metamorphosis
this arch becomes a ring
of cells surrounding the
intestine (Fig. 272).

The rudiment of the
cerebral ganglia becomes
detached from the cerebral
pit, and the cells forming
the apical plate degenerate,
cast off their cilia, and dis-
appear (Fig. 273). The loop
of the intestine becomes
very long, so as to extend
upwards parallel to the left
side of the stomach.

The metamorphosis of
the Veliger into the mussel
takes place with startling
rapidity ; it is as sudden as
the change which converts
the late free - swimming
larva of Polygordius into
the adult worm. As in
that case, so here, the velar
cells die and are cast off,
the larval muscles break up
and disappear, the whole
anterior region in which
the mouth was situated shrinks, and the cells forming the mouth
cone degenerate and disappear. The result of this change is to bring
the mouth and the anterior adductor closer to one another, and thus
to swing the foot round so that its apex points forwards instead of
downwards. The rows of gill papillae are swung round from a vertic;il

Fi<;. 273. — Sections through the cerebral pit of
Veliger larvae of Drtixsi'iixic {i<>lyni<ir/ih(!. (After
Meisenheimer. )

A, longitudinal section through (lie \\\\ nf a larva, in
which the apical plate is fully developed. 13, longitudinal
section through the pit in a lanain which apical plate i*
degenerating. C, transverse section through the anterior
part of the pit, in a Veliger to show its bilobrd Character.
a. I', apical plate; c.;/, rudiment of cerebral ganglion; r./i,
cerebral pit.

344

IN VEETEP.BAT A

CHAP.

to a horizontal position, and the loop of the intestine is straightened
out.

After metamorphosis the labial palps, so characteristic of the
adult mussel, are formed in an amazing manner. The cerebral pit,
from which the rudiments of the cerebral ganglia have been separated,
flattens out and forms two lateral bands of ciliated epithelium above
and at the sides of the mouth. These develop into the upper and
outer labial palps, while downgrowths from their inner ends give rise
to the inner and lower labial palps (Fig. 276).

The shell begins to alter its larval shape by a preponderant growth
of its posterior and lower angle, and by a certain amount of growth

FJG. 274. — Horizontal section through the anterior portion of an old Veliger of D-rci

polymorpha in order to show the differentiation of the cerebral ganglia from the
cerebral pit. (After Meisenheimer. )

r.g, cerebral ganglion ; c.p, cerebral pit; oes, oesophagus ; jiZ.jr, rudiment of pleura! ganglia ;

*Ii, shell ; V, velum.

of its anterior angle also. The gill papillae grow into long filaments,
which become locked together by the longer cilia on their lateral
faces. The development of an additional outer row of gill filaments,
and the bending up of the ends of the filaments to form the reflected
portions of the gill lamellae, take place later in life (Fig. 275).

The rudiments of the kidneys acquire cavities. The ring of cells
surrounding the intestine becomes double and the two layers separate
from one another, the cavity between them being the pericardium,
i.e. the coelom. The cavity of the heart is the space between the
inner of these layers and the intestine. The kidney becomes U-shaped,
and the inner limb of the U on either side (which will form the
ureter) coalesces with the corresponding part of the other kidney so
as to form a transverse space beneath the intestine. Into this space
opens, on either side, a diverticulum of the mantle-cavity, and in this

ix MOLLUSCA 345

way the external opening is formed. The greater part of the ureter

a

D

si

r.f

FIG. 275. — Side views of two young specimens of Drcisseiisin /».li/nioi-/>ln/ niter tlic
metamorphosis has taken place. (After Meiseiiheiiner. )

A, young specimen in which the shell retains the shape it possessed in the veliger. Ji, older
specimen in which the shell is beginning to assume its adult proportions, a, anus; <«!il.<i, anterior
adductor muscle ; mlil.p, posterior adductor muscle ; In; rudiments of gills ; <:y, cerebral ganglion ; c.p,
eerebral pit; /, foot; H, lieart ; /<>•/), liver; 7,-, kidney; l.p, labial palp; uf, otneyst ; per, pericardium ;
JLIJ, pedal ganglion ; r.f, retractor of foot ; st, stomach ; r.it, visceral ganglion.

is therefore not ectodermal but coelomic in origin. The limb of the

346

INVEETEBRATA

CHAP.

kidney which was originally the outer limb, bends inwards and fuses
with the lower part of the pericardium, and here the reno-pericardial
canal is formed (Fig. 277).'

m.c.

,V

DCS

m.c

FIG. 276. — Horizontal sections through the anterior portions of three just metamorphosed
specimens of Dreissensia polymarpha in order to show the transformation of the
cerel>ral pit into the labial palps. (After Meisenheimer. )

A, specimen in which the velum is just bring thrown oft'. B, old specimen in which the velum is
already discarded, in which the cerebral pit is beginning to open out. C, specimen in which the cerebral
pit has given rise to two ciliated lobes, r.</, cerebral ganglion ; <•.}>, cerebral pit; l.p, labial palps ; ni.i;
nnntle-cavity ; ues, oesophagus ; V, discarded velar cells.

The genital organ arises from a median ventral strip of the
pericardia! wall, in front, just between the openings of the reno-
pericardial canals. It consists of peculiar large cells with pale nuclei.
These cells multiply, become detached from the pericardial wall, and

IX

MOLLUSCA

347

inl

Ik

B

m.c

e.o

e.o

FIG. '111. — Diagrammatic transverse sections of young specimens of Ureis-iensii* polymorpha
in order to illustrate the development of the kidney. (After Meisenheimer.)

A, the kidney a round sac. B, the kidney assumes a U -shape— the outer limb develops into the
glandular portion, the inner Hint) into the ureter. C, the outer liinli beronifs lient inwards toward
the middle line. D, the two inner limbs— the rudiments i>r the ureters fuse in the middle line. E, the
internal and external openings are formed. f.<>, external opening of the kidney ; hit, intestine ; i.n, in-
ternal opening of the kidney ; I.I.-, left kidney ; m.c, mantle-cavity ; r.k, ri.uht kidney ; r.p, reno-peri-
cardial canal; ur, ureter.

348

INVERTEBRATA

CHAP.

divide into masses which, in the latest stages examined by Meisen-
heinier, are found beneath the pericardium and lying not far from
the lateral ectoderm on each side. The formation of the genital ducts
was not observed by him (Fig. 278).

per.gl

\Vl-

FIG. 278.— Transverse section through a young Dreissensia polymorpha in order to show
the origin of the genital organs. (After Meisenheinier. )

G, median mass of genital cells forming a thickening in the floor of the pericardium ; II, heart ;
int, intestine ; A:, kidney ; per.gl, pericardial gland ; per, pericardium ; r.ji, reno-pericardial canal.

Our account of the development of Dreissensia is now complete.
We must pause, however, and glance at what is known of the develop-
ment of other Pelecypoda before considering the development of the
highest Mollusca.

OTHER PELECYPODA

The development of no other Pelecypod has been worked out with
anything like the same completeness as Dreissensia. What we know
of other life-histories are mainly bits and scraps. From the accounts,
however, given by Horst (1882) of the development of Ostrea, by
Drew (1906) of that of Pecten, by Hatschek (1885) of that of Teredo, by
Sigerfoos (1895) of that of Pholas, and by Loven (1848) of that of
Oardium, we can only conclude that the development of all these forms
is practically identical with that of Dreissensia. The figures given of
the veliger larvae are so similar that one would almost be driven to con-
clude that there is a veliger larva of definite type common to all marine
Pelecypoda, and that the differentiation of the various genera from one
another takes place during post-larval life. Indeed, the researches of
Stafford (1910) on the veliger larvae found in the lagoons of Prince
Edward Island, and off the New Brunswick coast, have gone far to
bear out this conclusion. Amongst other things he has shown that
the late veliger larva of Ostrea virginiana possesses a well-marked
foot which is used for locomotion in the early post-larval stages,
before the definitely fixed life of the adult is assumed (Fig. 279).

IX

MOLLUSCA

349

The only point which requires some comment is the description
given by the earlier workers of the segmentation stages. Thus
Horst (1882) and Hatschek (1883) both describe the endoderm as
represented by one huge ruacromere, which buds off the micromeres
which give rise to the ectoderm ; instead of there being, as in all
other Mollusca, four rnacromeres. There is strong ground for
believing that this is a misinterpretation, and that in all cases four
macromeres are really formed, but that, as is the case with Dreis-
sensia, one is much larger than the rest.

To the statement that the development of Pelecypoda, up to the
veliger stage, pursues a uniform course in all genera, two marked
exceptions must be made. The first of these concerns the group of
the Protobranchiata, including
the genera Nucula, Leda,
Yoldia, etc., whose develop-
ment has been studied by
Drew (1899, 1901).

In this group the velum
acquires enormous dimensions,
and consists of circles of large
vacuolated cells placed one
above the other, forming a
barrel-shaped structure. The a'dd.c
first and last circles bear
numerous small cilia all over
their surface, and the central
three circles have each a narrow
band of long cilia (Fig. 280).

A sagittal section through this

FIG. 279. — The late Veliger larva of Ostrea
rin/hiiaiia, viewed from the side. (After
Stafford.)

iidd.a, anterior adductor muscle ; mkl.p, posterior
adductor muscle; In; rudiments of gills; /, Coot ; 7/c/i,
lobes of liver ; ot, otocyst ; V, retracted velum.

extraordinary structure reveals
inside it a saddle-shaped shell
gland, a long narrow storno-
daeum leading up to a stomach,

and a cerebral ganglion arising in Yoldia as a pit in front of the
apical plate (Fig. 281). The foot appears later, and when the meta-
morphosis occurs and the velar cells are cast away, the cilia covering
the foot are sufficiently powerful to enable the animal to glide over
the mud in which it lives before any burrowing movements are
carried out. The general plan of the development is therefore the
same as in Dreissensia.

At the other pole of variation are freshwater forms like Cydas,
Pisidium, etc., and the family of the Unionidae, where the early
stages of development are passed between the lamellae of the gill of
the mother, and where is therefore no free-swimming stage and
neither prototroch nor velum is developed.

In Ziegler's account of the development of Cydas (1885) it is
stated that there is only one large macromere from which all the
micromeres are budded off. As we pointed out above, this is probably

350

INVEETEBEATA

CHAP.

a misinterpretation of the early stages of development. Cychts is
further remarkable for the fact that the coelom makes its appearance
as two vesicles situated at the sides of the intestine. These vesicles
become constricted into dorsal and ventral halves, but they meet one
another both above and below the intestine, and hence, in another

FKJ. 280.— The Veliger larva of

liii/iitii/n, about three days oM. (After
Drew. )

a. /i, apical plate ; lij, position of blastopore ;
V, velum.

FIG. 281. — Longitudinal sagittal section
of the Veliger larva of Yuliliu lima/nlit.
three days old. (After Drew.)

ii. ji, apical plate ; c.g, rudiment of cerebral
ganglia (representative of cerebral pit); s.g,
shell ^land; t>t, stomach; stow, stomoclaeum ;
V, velar fells.

way, the same end results as that attained in Dreissensia. The space
between dorsal and ventral halves forms the auricle of the heart, that
between the vesicles and the intestine forms the ventricle (Fig. 282).
The Unionidae give rise to an extraordinary larva, known as
a Glochidium; it is devoid of mouth, velum, and foot, but provided
with a bivalve shell, and the lower borders of the valves are each

ix MOLLUSC A 351

provided with a sharp, inturned tooth. This larva is capable of only
a few spasmodic flappings of the valves of the shell, which propel it
through the water for a short distance. It is ejected from the gills
by the parent when a freshwater fish happens to pass in the vicinity,
and a successful larva contrives to fix itself on the gills or fins of the
passing fish by grasping them by means of the valves of the shell. The
bite of the valves stimulates growth of the soft vascular gill, so that
the Glochidium is soon enclosed in a cyst in which it completes its
development, and from which it emerges only when it has attained
the adult condition (Fig. 283).

The best account of the early development of Unionidae has been
given by Lillie (1895), and the most recent worker at the post-larval

-per

. o nay

int

-Sr^*- <^r^> Z^K^

—our

int

FIG. 282. —Diagrams illustrating the development of the pericardium in t'yvlus and
1 ) reissensia. (After Meisenheimer. )

A, development of pericardium in Cydiis. B, development of pericardium in Drciw.nsia. rmr, space
which forms the auricle of the heart; //, heart; int, intestine ; i«:r, pericardium.

development is Harms (1909). Lillie's account is interesting in
making it quite clear that, in spite of its aberrant appearance, the
development of the embryo of Unio conforms to the scheme given for
Dreissensia. There is, it is true, no prototroch, and the first quartette
of niicromeres divide only once or twice and form the " head vesicle."
On the other hand, as in Dreissensia, the first sornatoblast, 2d (X), is
enormous, and it divides in exactly the same way as in Dreissensia.
The group of small cells along its lower edge (Xj-x5) give rise to
what Lillie calls the ventral plate, a thickened region of the ectoderm
from which the foot is formed in post-larval life. There is a primary
inesoderm cell, 4d, which divides into right and left halves, from each
of which a packet of cells is formed, parts of which break up into
rneseuchyme. The shell gland is enormous and the endodermic
rudiment very small. As the shell gland becomes everted the

352

INVERTEBEATA

CHAP.

endodermic rudiuieut is invaginated and the blastopore closes, hut
the stomodaeum remains as a thickened plate of ectoderm during
the Glochidiuni stage. Rudiments of three pairs of ganglia are
sometimes present (jAnodon), and sometimes not (Unio*). On each
side the mantle-lobe bears three sense cells with long sense hairs.
There is a powerful adductor muscle connecting the valves of the
shell.

In the post-larval life the most marked feature is the modifica-
tion of the cells forming the larval mantle. These cells develop into
huge vacuolated columnar structures which actually absorb and
digest fragments of the blood cells and other tissues of the host

FIG. 283. — Glocliidium — larva of Margaritana with widely opened valves, viewed as a
transparent object from the dorsal surface. (After Harms. )

mlil, adductor muscle ; l>y.f, byssus thread ; cil, ciliated patch on the ventral surface ; sh, larval

shell ; st, stomach ; /, teeth of shell.

which enter the mantle-cavity of the parasite. The cells destined to
form the adult mantle arise from the apices of the two mantle-grooves
and spread downwards, displacing the larval mantle cells, which are
eventually shed (Fig. 284). We can only compare these rudiments
of the adult mantle to the imaginal discs of insects. The single larval
adductor muscle disappears and is replaced by the adult adductor,
of which sometimes the anterior and sometimes the posterior is the
first to be formed. The foot, gills, and otocysts arise exactly as in
Dreissensia. The coelom arises as two little packets of cells, one
on each side, closely attached to the ectoderm, from which Harms
supposes them to have been derived ; but this view, for reasons given
above, we cannot accept. The later development of these rudiments
is exactly the same as in Dreissensia ; the main mass on each side

IX

MOLLUSCA

353

hollows out to form the kidney, whilst a band of cells grows out
from each and forms a ring round the gut, splits into two layers,
and forms the pericardium.

The accounts of Harms and Lillie leave no doubt in the mind that
in the embryo of the Unionidae we are merely dealing with an
ordinary Pelecypod veliger modified for a parasitic existence.

int

a.m.

trv

m.c

FIG. 284. — Transverse section of a Glochidium larva of Unio which is already fixed in
the tissues of its post. (After Harm. )

'i. HI, cells which will form the adult mantle ; int, intestine; /./», vacuolated c-i-lls of larval mantle,
which absorb food material from the host ; m.e, mantle-cavity ; p.y, rudiments of pedal ganglia ; i, teeth
of larval shell.

CEPHALOPODA — Loligo, Sepia

We must now turn to the study of the embryology of the highest
Mollusca, the Cephalopoda (lit. head-footed), so called because the
fore part of the foot has grown into a frill surrounding the head.
Two genera are represented by common species, both on the English
coasts and in the Mediterranean ; these are Sepia officinalis and
Loligo vulgaris. So far as is known, the development of both pursues
a practically identical course. We shall select Loligo as a type for
special study, because its development has been more completely
worked out, and because species of this genus are common on the
American coast ; but we shall not hesitate to fill up lacunae in our
knowledge of the development of Loligo by the description of corre-
sponding stages from the development of Sepin, when these are
better known.

The eggs of both genera, like all Cephalopod eggs so far described,
contain an abundance of yolk, the cytoplasm being mainly restricted
to a small disc at the animal pole of the egg, in which the nucleus is
VOL. i 2 A

354 INVERTEBKATA CHAP.

situated. The Cephalopod egg is, in fact, the beau ideal of a telo-
lecithal egg. The egg of Sepia is nearly spherical, about the size of
a pea ; it is enclosed in a tough black chorion of the consistence of
india-rubber, difficult to remove. The egg of Loligo, on the contrary,
is about the size of an apple pip, and is of an elongated oval shape.
Many eggs are laid together immersed in a somewhat tough jelly,
which can be partly dissolved by exposure to the action of Eau de
Javelle for fifteen minutes.

For the study of segmentation stages surface views are essential,
and for this purpose the most superficial layer, including all the
cytoplasm, is removed from the animal pole of the egg by means of
a sharp knife, and the skin thus obtained is spread out flat. Even
when sections are desired it is inadvisable to endeavour to cut
through the whole mass of yolk ; only a small part of the upper half
of the egg should be removed and cut into sections.

The segmentation of Sepia has been carefully described by Vialletou
(1888). Miuchin began a renewed study of the subject and made a
series of exquisite preparations from eggs preserved in Hermann's
fluid, which, however, he did not describe ; but these have been
described by Koeppern (1909), and his results confirm in every detail
those of Vialleton, whose account we follow here. No such ex-
haustive account of the early stages of development of Lnligo is
available, but, from what is known of it, it agrees with that of
Sepia in every particular.

According to Vialleton, then, the cleavage of the egg of Sepia is
meroblastic, that is to say, it is only the protoplasmic end of the egg
which is divided by the cleavage furrows, the yolk being quite un-
affected. When the nucleus has divided into four, and two cleavage
furrows at right angles have been formed, we have obviously a stage
which corresponds to the stage of division of other Molluscan eggs
into four macromeres.

The next cleavage furrow is a circumferential one and cuts off four
inner cells, termed blastomeres by Vialleton, from four outer large
cells whose lower ends fade into the yolk, which he terms blasto-
cones. This stage corresponds roughly to the stage of the formation
of the first quartette of micromeres in other Molluscan eggs, but no
one has attempted to work out the cell-lineage in a Cephalopod egg,
and it will become obvious that many more cleavages are necessary
to separate one from another the specific materials of the germinal
layers than is the case with the vastly smaller eggs of other Mollusca.
For example, in the 32-cell stage of Sepia (Fig. 285), if the blasto-
cones be regarded as corresponding to the macromeres, it is obvious
that there must be at least 20 macromeres and only 12 micromeres,
whereas in a normal Molluscan egg there would be 4 macromeres
and 28 micromeres in the 32-cell stage.

By further radial cleavage furrows the number of blastocones is
greatly increased, and by new circumferential furrows the inner
portions of these are continually cut off as new blastomeres, whilst

IX

MOLLUSCA

355

the already existing blastomeres undergo division, and in this way
a one-layered sheet of cells, or " blastoderm," becomes spread over
the upper surface of the egg.

When the blastoderm has extended so as to form a sheet of cells
covering about one-eighth of the surface of the egg, the formation of
ne,w blastomeres from the blastocones ceases : these latter now appear
as a series of narrow, spoke-like pillars radiating from the blastoderm
as a hub. The basal portions of these spokes become narrower and
narrower, as their nuclei wander farther and farther away from the

• y

• K-

FIG. 285. — Segmenting egg (32-cell stage) of Scpiii nj/fi-iiin/ >'.•>• viewed from the animal pole.
(Alter Koeppern, from Minchin's preparations.)

')/<•, blasfcoconi- ; '</»/, blastomere.

1 tlustoderin, till they become mere threads. Finally the portion with the
nucleus separates altogether from the blastoderm and begins to divide,
and in this way a membrane is formed consisting of a single layer
of extremely flattened cells, which rapidly extends all over the
yolk ; it extends also underneath the blastoderm so as to cover the
yolk there also. This sheet of cells is termed the yolk-membrane ;
it has been rightly compared to a portion of the endoderm. Its cells
exercise some digestive influence on the yolk and gradually change
it into a form that can be used for the nourishment of the embryo.
But no part of this yolk-membrane is incorporated in the permanent
epithelium of the mid - gut. The cells from which the mid-gut
epithelium will be formed, arise later by divisions of the most

356

INVERTEBKATA

CHAP.

peripheral blastomeres of the blastoderm, at right angles to the surface.
These divisions take place along what afterwards are seen to be

lie

the posterior and lateral edges
of the blastoderm. In this way
an incomplete ring of what are
called " lower layer cells " is
formed, which former observers
have termed niesoderm but which
we may term mesendoderm.
Lankester (1875) maintains that
there is a " primitive streak "
in the segmenting eggs of Cephalo-
poda, by which he means a re-
stricted area of the surface over
which the proliferation of cells
which gives rise to the mesendo-
derm takes place. A priori this
is very likely, although so far
this observation has not been
confirmed. This mesendoderm
grows inwards under the blasto-
derm to a considerable extent,
but does not invade, except in
the form of a few loose scattered
cells, its front edge or its centre.

The formation of definite
organs in the embryo of Lolif/o
has been worked out in com-
paratively recent times by Korschelt (1892) and by Faussek (1900).
These workers found that Hermann's fluid, and similar mixtures
containing osmium tetroxide, render the tissues too brittle for section-
cutting although giving excellent histological detail. They therefore
employed picro- sulphuric acid and Terenyi's fluid, which gave
excellent preservation of form, although the histological detail is
not so perfect as that obtained by the use of Hermann's fluid.

The first organ to make its appearance is the shell gland. This
appears as a heart-shaped area of columnar ectoderm in the mid-
dorsal line. This thickening in fact occupies the apex of the egg ; in
front of it is what we may call the anterior slope, behind it the
posterior slope. Soon an invagination appears in the centre of this
thickening ; but, as Lankester long ago pointed out (1875), this does
not correspond to the invagination of the shell gland which we
encounter in other Molluscan embryos. That invagination precedes
the condition of the gland when it is a saddle-shaped area, and
lasts only a short time, but the iuvagination in the shell gland area
of a Cephalopod lasts throughout life ; it constitutes, in fact, the
shell-sac which encloses the shell (a horny pen in Loligo, but a
complex calcareous structure in Sepia). From a comparison with

FIG. 286. — A portion of the margin of the
blastoderm of the egg of Syria officinal in
at the conclusion of the process of seg-
mentation ; to show the transformation
of the blastocones into cells of the yolk-
membrane. (After Koeppern, from
Minchin's preparations. )

lilr, blastocones; .(/.«.<', yolk-membrane cells.

IX

MOLLUSCA

35*7

the primitive genus Nautilus, we know that this covering in of the
shell by mantle flaps is a secondary phenomenon which was not
present in the earlier Cephalopoda.

A

' rn.c.

FIG. 287.— Two sections through the edge of the blastoderm of Sepia officinalis in different
stagi-s of development ; to illustrate the development of the lower layer cells. (After
Koeppern, from Minchin's preparations.)

A, Younger stage. B, Older stage. A is more highly magnified than B. me, mesoderm, i.e. lower

layer cells ; i/./n.f, yolk-membrane cell.

The eyes now appear as shallow cups on the sides of lateral
protrusions of the body, which may be termed eye-stalks. The edges
of the Cephalopod shell gland constitute, as in other Mollusca, the
rudiment of the mantle, and underneath them appears a groove,

FlO. 288. — Two early embryos of Lufii/u ruli/n ris. (After Korselielt.)

A, An embryo seen from the posterior side. B, A slightly older embryo >een IVoni the anterior
side, ar, rudiments of anus; HI./, mantle-fold ; o.c, optic cup; o.it, optic stalk; .«..-•, shell-sac ; stom,
stomodaeum.

deepest behind, which is the rudiment of the mantle-cavity. Just

within this groove two buds appear to the right and left of the

•middle line ; these are the rudiments of the gills : whilst below them

appear two pairs of ridges converging towards the ventral surface and

358

INVEKTEBEATA

CHAP.

o.st

or/-

constituting the rudiment of the hind foot or funnel. These are
termed the anterior and posterior funnel folds respectively. The
rudiments of the fore foot, the arms, appear as a series of thickenings
on the lower edge of the blastoderm (Figs. 288, 289).

Whilst these changes have been going on, the first trace of the
mid-gut makes its appearance as a thickening of the " mesendoderm "
on the posterior slope of the egg ; whilst the stoniodaeurn appears as
an invagination in the middle line of the anterior slope of the embryo.
In the endodermal thickening a cavity is formed by the
separation of its constituent cells from each other. This cavity is
at first closed internally merely by the yolk -membrane ; but it soon
independently acquires its own internal wall, whilst externally it

raises the ectoderm into a slight
papilla, the anal papilla, at the
apex of which the anus appears a
little later. There is no procto-
daeum. Before the anus is per-
forated the incipient mid-gut gives
off a diverticulum which is the rudi-
ment of the ink gland (Fig. 290, B).
The stoinodaeum is at first a
shallow cup, but it soon extends up
towards the mid-dorsal line and past
it, where, in a much later period of
development, it fuses with and opens
into the mid-gut. The radula sac
appears as a ventral outgrowth of
the stoinodaeum, and a still more
ventral outgrowth is the rudiment
of the salivary gland. The oto-
cysts now arise as open pits near
the junction of the anterior and
posterior funnel folds. These
two pairs of folds, as already noted,
are the rudiments of the funnel.
In this stage the rudiments of the three principal pairs of
ganglia arise. The cerebral ganglia appear as long streak-like
ectoderniic thickenings running below the eyes ; the pedal ganglia
as much shorter streaks parallel to the hindermost portions of these
and above them, extending to the otocysts ; and finally the pleura!
ganglia are represented by short vertical streaks extending up
towards the mantle. The shape of the rudiments reminds one of the
band-like condition of the ganglia found in Nautilus (Fig. 291),
and we may add that the appearance of the funnel as two un-
connected ridges also recalls its condition in Nautilus.

The first trace of the genital cells appears in this stage as a
packet of large pale cells with pale nuclei, situated on the posterior
aspect of the embryo between the rudiment of the gills (Fig. 297, A).

dff

FIG. 289. — Embryo of Loligo vvlgaris
seen from the posterior side at the
conclusion of the period of develop-
ment, termed by Faussek Stage 1.
(After Faussek. )

«., anus ; ti.f.f, anterior funnel fold ; ric,
rudiment of arms ; /<;•, gill rudiment ; »/./,
mantle fold ; p./.f, posterior funnel fold ; o.st,
eye-stalk ; «t, otocyst ; s.s, shell-sac.

IX

MOLLUSCA

359

mes

FIG. 290. — Two sagittal sections of early embryos
of Loliyo vulgar is in order to illustrate the
first formation of organs. (After Faussek.)

A, Staj;e in which the endoderm is first visible as a
differentiation of the mesoderm. B, Stage in which the
ink sac is formed, end, endoderm ; i.s, ink sac ; w \
mesoderm s..v, shell-sac ; stem, stomodaeum ; y.m, yolk-
membrane.

360

INVEKTEBRATA

CHAP.

As development proceeds the upper portion of the egg, covered by
the blastoderm, begins to be separated by a constriction from the
lower part, which consists merely of yolk covered by the yolk-
membrane, and so we are enabled
to distinguish between " embryo "
and yolk-sac. It must be remem-
bered, however, that a considerable
portion of the yolk is contained
within the confines of the embryo;
this is known as the internal yolk-
sac, and is disconnected from the
C9 external yolk-sac, which appears
as an appendage. The two are, of
course, joined by a neck of corn-
er HL nmuication.

ost

r

oc

B

FIG. 291. — Embryo of Lulif/o vulgaris seen
from the side and behind in order to
illustrate the development of the ganglia.
The embryo is younger than that repre-
sented in Fig. 289. (After Fanssek.)

A, Embryo seen from behind. 13, Embryo
seen from the side, n.f.f, anterior funnel folds ;
ar, rudiments of arms ; In; rudiment of gill ; c.g,
rudiment of cerebral ganglion; on, eye-cup; o'.st,
eye-stalk ; ot, otocyst ; />././, posterior funnel
folds ; /..-/, rudiment of pedal ganglion ; s.s, shell-
sac ; <:<i, visceral ganglion.

Fi<;. 292. — Embryo of Lnliyti nili/nri* in
the stage termed by Fanssek Stage 2,
when the embryo begins to be grooved
oil' from the yolk-sac ; posterior view.
(After Korschelt.)

Li'ttiT.s as in previous figure. In addition,
it. p, anal papilla ; r.f, retractor muscle of
funnel ; t.ai; tentacular arms.

When the grooving off of the external yolk-sac has become
distinct, many other changes take place. The eye-stalks grow in
length, while the eye-pits become closed, and the inner segment of
the lens is developed as a secretion from the anterior wall of each
pit. The otocysts also become closed and sink into the ridges which

MOLLUSCA

361

are the rudiments of the funnel. The retractor muscles of the
funnel appear as two ridges which stretch from the middle of the
funnel, where anterior and posterior funnel folds have united,
upwards to the edge of the mantle. The mantle edge extends over
the rudiments of the gills, and the mantle cavity deepens ; whilst
the shell-sac closes, and the central region of the mantle becomes
arched up so as to constitute a visceral hump. The rudiments of
the arms lengthen ; those of the tentacular arms exceed the others

FIG. 293. — Sagittal sections of two embryos of Loliyo ntlgaris to illustrate the formation

of internal organs. (After Korschelt. )

A, Section of younger embryo with incomplete alimentary canal. 13, Section of older embryo in
which stomodaeum and niid-^ut have joined, a, anus ; <\g, cerebral ganglion ; e.y.a, external yolk-sac ;
/, funnel ; //;,, tin rudiment ; //, heiirt ; int., intestine ; i.x, ink sac ; t.J/.s, internal yolk-sac ; m.c, mantle-
cavity ; HI./, mantle-fold ; u, mouth ; ut, otocyst ; ji.ij, pedal ^an^lion ; j,Kr, pericardium ; r.s, radulasac ;
sal, salivary gland ; s.s, shell-sac ; stout, stomodaeum ; t:g, visceral ganglion ; y.-in, yolk -membrane.

in length. The rudiments of the ganglia become constricted off
from the thickenings of the ectoderm ; that part of the thickenings
giving rise to the cerebral ganglia which lie beneath the eyes, becomes
infolded and gives rise to the so-called white bodies (Fig. 292).

The internal changes which occur are best made out by combining
the views obtained by sagittal sections with those obtained by
horizontal sections through the embryo. The most marked features
of the stage which we are discussing are the appearance of the
coelomic cavities and of the blood spaces, both of which arise as

362

INVEKTEBKATA

CHAP.

5.5

P

'.5

splits in the mesoderm. The coeloinic cavities contain a clear fluid,
and have a definite epithelial arrangement of the cells forming their
walls ; whilst the blood spaces contain an albuminous serum which
stains, and their walls are often irregular and in some places formed
only by the yolk -membrane.

The coelom arises as two vesicles lying beneath the mid-gut.

Each of these vesicles
becomes divided by a con-
striction into a dorsal part,
which is the rudiment of
the pericardium, and a
ventral part, the rudiment
of the kidney ; the connec-
tion between the two,
though narrow, persists,
and forms the reno-peri-
cardial canal.

Beneath the shell-sac,
on the posterior slope of
the embryo, a wide blood
space arises whose cavity is
traversed by cords of mesen-
chyme. This is the posterior
sinus (Fig. 294). It ex-
tends anteriorly round the
sides of the gut and there
constitutes the two forks
of the vena cava. From
this a branch extends into
the rudiment of the gill,
which is the beginning of
the branchial heart. In
front, these forks unite
beneath the gut to form
the unpaired vena cava.
The heart arises independ-

A, The more posterior ; B, the more anterior section. ently of this sillllS as tWO

7<r, Kill; I,,:!,, rudiment of branchial heart ;-•„,, rudiments ]lol]ow tnUpo lvim>- intpr-
of coelom ; II, rudiments of systemic heart ; iut, intestine ;

p.s, posteriorblo.nl sinus; s.s, shell-sac; v.c, vena cava. lially between the COeloillic

rudiments. Behind, these

tubes unite to form the ventricle, but in front, where kidney and
coelom join, they diverge so as to form the auricles (Fig. 295).

In the next period of development, the end of which is represented
in Fig. 296, the embryo becomes as large as the external yolk-
sac, and the funnel is definitely constituted by the union of the free
edges of the folds in the mid-ventral line. The arms have now
acquired suckers and have extended round the head to the mid-
dorsal line, so that the encircling of the head by the fore foot is

COS

cee

vc

FIG. 294. — Two diagrammatic transverse sections
through a young embryo of Lul/'//n rit/</{ii'ix to
illustrate the origin of the coelom and the blood
cavities. (After Faussek.)

IX

MOLLUSCA

36:

completed. The anterior chamber of the eye is formed as an ecto-
dermic fold, which arises from the base of the eye-stalk and encloses

me.

H

-tic,

it. In this way the
outer surface of the adult
head is formed and the
eye-stalks are no longer
prominent. This en-
veloping fold we may
term the corneal fold.
From the spot where the
primary eye vesicle closed
the rudiment of the outer
segment of the lens is
formed as an external
secretion. The eyelids Per
are constituted by a pair
of folds similar to those
which wall in the anterior
chamber, but lying out-
side the latter. Lying-
inside the anterior
chamber is still another
pair of folds which con-
stitute the iris.

The alimentary canal,
which had become a
completed tube in the
previous period, now
shows further develop-
ment. The radula sac
becomes sharply marked off from the stomodaeum. In front of it two

a.

/,-

brh

m.c.

FIG. 295. — Diagrams of three transverse suctions
through an emliryo of Ln/fi/n nil</ttris, much older
than that represented in Fi-. 'J'.M. (After Fanssi-k.)

A, The most posterior; C, the most, anterior of (lie three
sections. Letters as in jnwions iimne. In addition, aur,
auricle; /,-, kidnr\ ; ,».,-, mantle-cavity; m.r. mant I^-VIMII ;
/»•/•, pericardium.

364

INVEETEBEATA

CHAP.

~fn

ventral diverticula grow out, which are the rudiments of the salivary
glands. The mid -gut becomes differentiated into a stomach
and an intestine, and the diverticulum which forms the ink sac
opens into the latter. The liver arises as two lateral outgrowths
of the stomach. The surfaces of these outgrowths become folded,
and this is the first indication of the formation of the liver tubules.
The coelom, which is already constricted into kidney and pericar-
dium, now increases greatly in volume. The two pericardial rudiments

fuse behind and enclose the two
rudiments of the heart ; these
latter likewise fuse together.
In front the pericardial rudi-
ments remain separate and are
applied to the paired rudiments
of the heart which here con-
stitute the auricles. The paired
portions of the pericardium
communicate with the kidneys
and give rise to the reno-
pericardial canals. Behind,
the single pericardium grows
backward and extends into
the growing genital organ,
which becomes divided up into
the genital folds. This portion
of the pericardium becomes,
later, divided off from that sur-
rounding the heart and forms
the genital coelom (Fig. 297).

The kidney sacs develop a
high columnar epithelium on
their inner walls, where they,
are in contact with the forks
of the vena cava ; the epithelium
lining their outer walls becomes
very thin. The posterior sinus
is reduced to very small
dimensions by the expansion
of the shell-sac, and is cut off from the vena cava. The portions
of the vena cava which extend into the gills and constitute
the branchial hearts, develop great thickenings of their walls on
one side. These thickenings, as experiment has proved, are excretory
in nature and consist of vacuolated cells ; they are covered
externally by thin peritoneal epithelium where they touch the
coelom. These are of course the appendages of the branchial heart.
The cartilage so characteristic of Cephalopoda is formed by the
modification of mesodermic connective tissue, and is first visible
in the neighbourhood of the foot. The chromatophores likewise,

FIG. 296. — Embryo of Loligo vulgar is at the
period when the funnel is formed, viewed
from behind. (After Korschelt.)

ar, arms ; i-n.f, i-orne il fold which envelops the
eye-stalk, and forms the outer chamber of the eye;
/, completed funnel ; /», tins ; in.f, mantli' i'd,ne ; or,
eye ; y.s, yolk-sac.

IX

MOLLUSCA

365

according to Faussek, are of inesodermal origin. During this period
the whole of the ectoderm, except that covering the inner surfaces of
the arms, undergoes mucous degeneration — i.e. the cytoplasm of its
cells degenerates into slime and is cast off. How the adult ectoderm
is regenerated Faussek was unable to determine.

B

vs. • .••. ••• ** ».••-
>.-1-.V... •: .••"•

Fic. '297. — Transverse sections of embryos of young cuttle-fish, illustrating two stages in
the development of the genital organs. (Alter Faussek. )

A, Section through young embryo of I.uli'jn nilijiiris, showing the first appearance of tin1 genital <vlls
in tin- mesoderin. B, Section through older embryo of >v/i/n "[liriindis, showing tin' migration of these
cells into a fold projecting into the coelom. ///•, rudiments of gills ; <ien, genital cells ; i/J\ genital fold ;
//. heart ; i/i.c, mantle-cavity ; p.n, posterior aorta ; jier, pericardium ; ji.x, posterior sinus ; x. -. >liell-sar.

At the time that the external yolk-sac is absorbed, a large
diverticulum, the spiral caecum, grows out from the stomach ; and
this circumstance, together with the enlargement of the internal
yolk-sac, into which some of the yolk from the external sac passes,
is responsible for the almost entire suppression of the cavities of the
kidneys and genital organs which takes place at this period. Later,
when the yolk is finally absorbed, the kidneys and pericardium

366

INVEETEBEATA

CHAP.

reacquire their cavities, and then the kidneys become fused together
in the mid-ventral line ; this fusion is characteristic of Loligo, and

does not occur in
Sepia. •

By ' far the most
complicated

organ

n

Fie. 298. — Two early stages in the
eye of L<>li<i<> rulijiiris seen in
( After Lankester, from l!;ilt'our. )

of, eye-cup; r, rudiment of retina.

levelopment of the

transverse section.

the Cephalopod is the
eye, the general features
of the development of
which have already been
described. Some details
may now be added. As
soon as the primary
eye pit closes the inner
segment of the lens
begins to be formed.

O

It first appears as a
thin cuticle spreading

w

y fx

Fit;. 299. — Sections through the developing eyes of young cuttle-fish to show the

development of the leus. (After Faussek.)

A, Section through the eye of Lulirjn rn/i/nri*. U, Section through tlio eye of .sv^/Y; oflirinnlin. c.e-ii,
Ifii^'c- cells (if (he corpus epitheliale ; r.c/i', sni.-ill cells of the jiei iphci-y nC I lie cm pus cpithcli;ile which
grow over the larger cells .-mil secrete the lilnes nl' the lens ; i.l, inner segment <>t' the1 lens ; ir, iris ;
?./, lens liliics.

over a considerable portion of the inner surface of the closed eye-
sac, but it becomes thickened at one point in the centre, and

IX

MOLLUSCA

367

projects inwards as a rod -shaped structure. The cells forming
this part of the wall of the eye -sac are enlarged and cubical,
whilst those forming the more peripheral portions of the eye-sac
wall are small. The large cells, which secreted the 'primary 'part of
the lens, disappear in the centre, probably as a result of lens secretion ;
towards the sides they persist as the characteristic cells of the corpus
epitheliale of the ciliary body. The further growth of the lens is

o.st.

cep

o.st

FIG. 300. — Transverse section of the eye of a nearly ripe embryo of ,SV///f <>/

( After Faussek.)

c.ep, epithelial body; c.ujji, small cells nf r.rp forming lens capsule; <:f, conical fold constituting
the outer wall of the outer chamber of the eye; K.I, thickening, the rudiment of the lower eye-lid ;

g.C, ganglion cells of the retina; i.rli, inner chamber of tl ye; i.l, inner segment of the lens; h;

iris; o.efc, outer chamber of the eye; o.l, outer segment of the lens ; u.xt, eye-stalk; v.c, visual cells nf
the retina ; n-.li, nicsodernuil rudiment nf the white body.

effected by means of the small cells forming the more distant portions
of the wall of the eye-sac. These cells grow forward on each side
towards the lens, as a kind of fold overspreading the large cells of the
corpus epitheliale; and by them the lens is added to, both in thick-
ness and depth.

The iris folds and the outer segment of the lens are formed before
the fold which walls in the anterior chamber of the eye, and constitutes
the corneal fold, is formed. The outer segment of the lens is formed
like the inner segment ; at first it is a cuticle which thickens in the

3G8 INVEETEBRATA CHAP.

centre, then the cells beneath this thickening disappear and it is added
to by the more lateral cells.

If this description be followed it is clear that the primary eye
vesicle, with its contained inner segment of the lens, corresponds to
the eye as we find it in Gastropoda; and that the outer segment of
the lens and the outer chamber of the eye are subsequent additions.
The ciliary body consists of the adpressed posterior wall of the outer
chamber and anterior wall of the inner chamber of the eye.

The hinder wall of the primary eye vesicle forms the retina.
This consists at first of a single layer of columnar ectodermal cells
with the nuclei at different levels, bounded externally by a basement
membrane. Laterally it is continuous with the layer of small cells
which forms the lens. Soon the single layer constituting the retina
changes into many layers of small rounded cells ; of these the outer
layers begin to pass outwards through the basement membrane, and
they constitute the nervous layer of the retina. From tbe innermost
layer of cells visual rods grow out (v.c, Fig. 300), pointing into the
cavity of the eye-sac; but these cells do not all undergo this transforma-
tion; alternating with the visual cells are cells which secrete pigment.
The inner portions of the visual cells, that is, the portions turned
towards the cavity of the eye-sac, and these pigment cells, alone retain
their primary position with regard to the basement membrane. The
nervous portion of the retina is thus seen to consist of two layers of
nuclei with a clear space between them (almost certainly occupied by
dendrites of the nerve cells), and the whole presents a striking analogy
to the layers of cells in the human retina, except that the layers occur
in the reverse direction so far as the incidence of light is concerned.

GENERAL CONSIDERATIONS ON THE ANCESTRAL HISTORY OF MOLLUSCA

When we review the account of the development of Mollusca
given in this chapter, certain facts stand out clearly. First, in the
early larvae of Patella, Dentalium, and Dreissensia we are evidently
dealing with a single type, and this type must be classed as a Trocho-
phore larva, similar in all essentials to the Trochophore larva of
Annelida. Therefore the common ancestral group from which
Gastropoda, Scaphopoda, Pelecypoda (and we may add Solenogastres)
spring, must have had a Trochophore larva. In a word, all Mollusca
are thus shown to be descended from an ancestor represented by the
Trochophore, i.e. the same ancestor as gave rise to the Annelida.

What, it may be asked, was the factor which caused two families
of the descendants of this ancestor to diverge so widely from one
another in structure ? We must surely look for this factor solely in
a divergence of modes of life. Now, the fundamental type of habits
common to all Annelida is a burrowing mode of existence; and from
that, coupled with a wriggling method of locomotion during their
occasional excursions into the upper water, we were able to deduce
the main peculiarities of their adult structure. But the habits of

ix MOLLUSCA 369

Mollusca do not lend themselves to such easy generalization. The
Pelecypoda and Scaphopoda burrow, the Gastropoda crawl, and the
Cephalopoda propel themselves by projecting squirts of water through
the funnel.

But if we take into account Drew's statement (1899) that Yoldia
—surely one of the most primitive of Pelecypoda, — when just meta-
morphosed, glides over the mud by means of its cilia, we might be
inclined to conclude that the primitive habits of the original Mollusca
consisted in crawling or gliding over the surface, in contradistinction
to the burrowing mode of life adopted by primitive Annelida. It is
highly probable that the most primitive living Cephalopod, Nautilus,
in which the constituent folds which make up the funnel are not
united, can flatten out this organ and crawl.

But if we are entitled to conclude that the Trochophore larva
represents the common ancestor of Annelida and Mollusca, we must
regard the various Veliger larvae as representing an anticipation of
adult conditions ; a telescoping of development, in all respects similar
to that shown by the post-trochophoral stages of development in
Annelids.

The Veliger of Gastropoda, with its spirally twisted shell, can
hardly represent an ancestral stage ; because, as we have seen, the
unequal growth of the mantle edge which causes the twisting is most
plausibly explained by the overbalancing of a tall visceral hump, such
as would surely occur in an animal crawling over uneven ground,
not in one which was free-swimming. The Veligers of Pelecypoda
and Scaphopoda exhibit in the free-swimming stage the distinguish-
ing adult characters of their respective groups. As has been mentioned
several times already, this reflection of adult characters into success-
ively early stages of life-history is a phenomenon which meets us
everywhere in embryology, and it is one of the most suggestive
features in the whole process of development.

Turning now to the development of Cephalopoda, it is at first
sight difficult to find any points of contact whatever between their
development and that of other Mollusca. Thus, the gills are amongst
the earliest organs to be formed in Cephalopoda, whilst they are the
latest in Gastropoda and Pelecypoda. All trace of the Trochophore
stage has been eliminated from Cephalopod ontogeny, and there is
nothing corresponding to the veliger stage. Even the early history
of the shell must be greatly hastened through, for the shell-sac and
shell gland are two different things. Lankester (1890) has pointed
out that, in the later stages of the development of the snail (Helix),
a large ventral protrusion of the foot filled with yolk is produced.
This he rightly compares to the external yolk-sac of the Cephalopod
embryo, for this certainly represents a median protrusion of the foot,
since the rest of the foot is formed all round it. We have here, -how-
ever, a case of analogous development, not of real homology, for the
heavily yolked egg of the asymmetrical snail has not been derived
from the heavily yolked egg of the Cephalopod, or vice versa.
VOL. i 2 B

370 INVEBTEBKATA CHAP.

If, and when, the development of Nautilus is worked out, we
shall probably gain points for comparison of the development of
Cephalopoda with that of other Mollusca ; in the meantime we can
only conclude that the accession of large stores of nourishment has
almost obliterated the traces of ancestral history in their development,
leaving only the most general resemblance in the formation of the
layers and the development of the sense-organs, as links between
them and other Mollusca. In fact, the reflection of the development
of organs which become important in adult life, into successively
earlier periods of development, termed by Lankester heterochrony,
has, in Cephalopoda, reached its maximum.

LITERATURE CONSULTED

Boutan. La Cause principalc de I'Asymetrie des Mollusques Gasteropodes.
Arch. Zool. Exp. , 3rd series, vol. 7, 1899.

Casteel. The Cell-lineage and Early Larval Development of Fiona marinu, a
Nudibranchiate Mollusc. Proc. Acad. Nat. Sci., Philadelphia, 1904.

Conklin. The Embryology of Crejudula. Journ. Morph., vol., 13, 1897.

Crampton, H. E. Experimental Studies on Gasteropod Development. Arch. Ent.
Mech., vol. 3, 1896.

Drew. Yoldia limatula. Mem. Biol. Lab., Johns Hopkins Univ., vol. 4, 1899.

Drew. The Life-History of Nucula dclphinodonta. Quart. Journ. Micr. Sc.,
vol. 44, 1901.

Drew. The Habits, Anatomy, and Embryology of the Giant Scallop Pectcn tcnui-
costatus. Univ. Maine Studies, Nov. 1906.

Drummond. Notes on the Development of PahuUna vivipara, with special refer-
ence to the urino-genital organs and theories of Gasteropod Torsion. Quart. Journ.
Micr. Sc., vol. 46, 1902.

Erlanger. Zur Entwicklung von Paludina vivipara. Morph. Jalirb.. vol. 17,
1891 92.

Erlanger. Zur Bildung des Mesoderms bei der I'a/iit/i/iti lir/jiam. Ibid. vol. 22,
1894.

Erlanger. Etudes sur le developpemeut des Gasteropodes pulniones. (1) Etude sur
le rein larvaire des Basommatophorcs. Arch. Biol., vol. 4, 1895.

Faussek, V. Untersuchungen iiber die Entwicklung der Cephalopoden. Mitt. Zool.
Stat. Neapel, vol. 14, 1900.

Harms. Postembryonale Entwicklungsgeschichte der Uniouidae. Zool. Jahrb. ,
(Abt. fur Out.), vol. 28, 1909.

Hatschek. Uber die Entwicklungsgeschichte von Terafo. Arb. Zool. Inst. Wien,
vol. 6, 1885.

Heath. The Development of IschnocMton. Zoo], Jalirb. (Abt. fur Out.), vol. 12,
1899.

Herbst. Uber das Auseinandergehen von Furchung und Gewebeszellen in kalk-
freieu Medium. Arch. Ent. Mech., vol. 9, 1900.

Heymons, R. Zur Entwicklungsgeschichte von Umbrella mediterranea. Zeit. f. wiss.
Zool., vol. 56, 1893.

Horst. De Ontwikkelingsgeschiedenes van de Oesler. Tijdschr. Ned. Dierk., Dec. 1,
1882.

Holmes. The Early Development of Planorlis. Journ. Morph., vol. 16, 1900.

Koeppern. Notes on Prof. E. A. Minchin's preparations of the early stages in the
development of Sepia. Proc. Roy. Soc. Edin., vol. 18, 1909.

Korschelt. Beitriige zur Entwicklungsgeschichte der Cephalopoden. Festsch. zum
70ten Geburtstag von Leuckart, 1892.

Kowalevsky. Embryogenie du Chiton polii, avec quelques remarques sur le
developpement des autres Chitons. Ann. Mus. Nat. Hist. Marseilles, vol. 1, 1883.

Lankester. Observations on the Development of Cephalopoda. • Journ. Micr.
Sci., vol. 15, 1875.

Lankester. Zoological Articles, Mollusca (rept. from Encyclop. Brit. 1890).

ix MOLLUSCA 371

Lillie. The Embryology of the Unionise. Joimi. Morph., vol. 10, 1895.

Lbven. Beitrage zur Kenntniss dor Mollusca Acephala Lamellibranchiata. Transla-
tion, 1879, from Able. Kang. Sehwed. Akad. Wiss., 1848.

Mazzarelli. Bemerkungen iiber • die Analniere der freilebenden Larven dci
Opisthobranchiern. Biol. Centrbl., vol. is, 1898.

Meisenheiuier, J. Entwicklungsgeschichte von Limit j.' iii</,<'intus, 1't. I. Zeit. f.
wiss. Zool., vol. 63, 1898.

Meisenheimer, J. Kntwieklungsgeschichte von Dreissensia polt/morp/ia. Zeit. f.
wiss. Zool., vol. 69, 1901.

Patten. The Embryology of Patella. Arb. aus d. Zool. Instit. der Univ. \Vien,
vol. 6, 1885.

Robert. Recherches sur le developpement des Troques. Arch. Zool. Exp. , series 3,
vol. 2, 1902.

Stafford. On the Recognition of Bivalve Larvae in Plankton Collections. Cont.
to Biology, Ottawa, 1910.

Sigerfoos. The Pholadidae : I. Note on the Early Stages of Development. Johns
Hopkins Univ. Circ., vol. 14, 1895.

Tonniges. Die Biklung des Mesoderms bei Paludina vivipara. Zeit. f. wiss. Zool.,
vol. 61, 1896.

Vialleton. Recherches sur les premieres phases du developpement de la Seiche
(Sepia officinalis). Ann. Sci. Nat. Zool., vol. 6, 1888.

Wierzejski. Die Entwicklungsgeschichte von Physa fontinalis. Zeit. f. wiss.
Zool., vol. 83, 1905.

Wilson. Experimental Studies in Germinal Localixation. (1) The Germ Regions
in the Egg of Dcntalium. (2) Experiments on the Cleavage-Mosaic of Patella and
Denlalium. Journ. Exp. Zool., vol. 1, 1904.

Ziegler. Die Entwicklung von Cyclas cornea. Zeit. f. wiss. Zool., vol. 41, 1885.

CHAPTER X
PODAXONIA

Classification adopted—

ir. , , . ( Sipunculoidea

Podaxonia (G-ephyrea nuda) { _.j . ,

' I Phoronidea

IN the old group of the Gephyrea, which used to be regarded as a
subdivision of the Annelida, there were included several families or
sub-orders of such diverse structure that it has been recently
customary to separate them entirely from each other and to regard
them as belonging to quite distinct phyla. Of these families one,
tbe Echiuroidea, is undoubtedly to be regarded as a modified group
of Polychaeta ; and about another, the Priapuloidea, nothing can be
said until the development has been worked out, and we know more
about the adult anatomy of its members. A third group, the
Sipunculoidea, constituting the Gephyrea uuda, agrees witli Annelida
and Mollusca in possessing a Trochophore larva, and hence must be
regarded as descendants of the same Ctenophore-like ancestor, from
which, as we have seen reason to believe, these two phyla originated.
They differ, however, from both Annelida and Mollusca in the fact that
the principal extension of the body takes place in a direction almost
at right angles to the line joining mouth and anus, aud further-
more in a ventral direction. Hence the name Podaxonia, coined for
them by Eay Lankester (1890) with his customary insight.

It is probable that the group of Ectoproct Polyzoa is allied to
the Podaxonia, but the full proof of that is a matter to be settled by
future investigation. The group of the Phorouidea, however, con-
stituting the old division of Gephyrea tubicola, is almost certainly
closely allied to the Podaxonia, of which it will be considered a sub-
division. Evidence in favour of this view will be offered in this
chapter.

PHASCOLOSOMA

The genus Phascolosoma has representative species on both sides
of the Atlantic. The cell-lineage and larval development of the

372

CHAP. X

PODAXONIA

373

American species P. gouldii has been worked out by Gerould (1907),
who also continued his results by work done on the European species
P. vulgare.

The eggs of the American species, when they mature, are dehisced
into the coelorn and pass into the nephridia. They are finally laid in the
sea and there fertilized. They are provided with a strong " chorion "
or "yolk-membrane," which persists until the close of embryonic and
the beginning of larval development. The spermatozoon penetrates
this membrane through a micropyle. After the eggs have been fixed
in picro-sulphuric acid, it is possible to dissolve the chorion by
exposing them to Laburraque's solution for two hours, and according
to Gerould no harm is done to the egg itself by this treatment.

The cleavage reminds us in many ways of that of Dentalium.
The egg divides into the usual four uiacromeres, but I) is, from the

Ir

IB

D 1C

IB

FIG. 301. — Early segmentation stages of the egg of Phascolosoma gouldii. (After Gerould.)

A, 4-cell stage viewed from tin- side. B. 8-cell stage viewed from the side.
C, S-cell stage viewed from above, ch, chorion ; p.li, polar bodies.

first, very much bigger than its sisters A, B, and C. It has, in fact,
five times the volume of any one of its three sisters. In the 8-cell
stage a first quartette of micromeres is formed, and these are
relatively large cells, as big as the smaller naacrorneres.

In the 16-cell stage la, Ib, Ic, and Id divide as usual into la1,
Ib1, Ic1, and Id1, and la'2, Ib2, Ic2, and Id2 respectively. These two
sets of cells are about equal in size, and they are larger than the
residual uiacromeres 2A, 2B, and 20. Of the second quartette of
rnicrorneres which, with these macromeres, form the lower half of the
egg, 2a, 2b, and 2c are small, but 2d and its sister cell, the residual
macromere 21), are both enormous and of about equal size. In
attaining the 32-cell stage, the upper eight cells of the egg Divide
equally, so that the quartettes of cells lqn, lq12, Iq-1, and 1q'-'2
are all of about equal size. So far as the second quartette of
micromeres are concerned, each divides into a small upper and lower
larger cell. The residual macromeres 2 A, etc., give off the third

374

INVERTEBRATA

CHAP.

la21

22

quartette of micromeres ; 3a, 3b, and 3c being formed first and 3d
later. They are all comparatively small cells (Fig. 302).

The upper half of
the egg continues to
divide more rapidly
than the lower half.
Iq11 divides into Iq111,
the apical cells, and
Iq112, which are the
so-called " peripheral
rosettes" or the An-
nelidan cross, whilst
the so-called " inter-
mediate girdle cells,"
Iq12, divide into Iq1-1,
the basal, and Iq1--,
the intermediate cells
of the arms of the

3A

3£

FLO. 302. — Later stage in the segmentation of the egg of
J'/ifisi-n/iinui/in i/iiitldii, viewed from the posterior aspect.
(After Gerould.)

' Molluscan cross."

Iq21 and Iq2- also each
divide, so that in each

Cells belonging to the second quartette are dotted; those belonging quadrant 01 the egg

there are four daugh-

to the third quartette are ruled with vertical lines.

ters of Iq'2, and these
cells are, of course, as in Mollusca and Annelida, the primary
trochoblast cells.

A la112

1M22

F'IG. 303. — Two views of the apical region of the segmenting egg of Phascolosoma

n/Igarc. (After Gerould.)

The apical and the prototrochal cells arc loft white. The " peripheral rosettes " or " Annelidan
cross " cells are covered with circles, whilst the " intermediate girdle cells " or " Molhiscan cross " are
ruled with horizontal lines. A, early stage. B, 4S-cell stage, p li, polar bodies.

These cells in Phascolosoma are very large and extend backwards
so as to overlap and cover the cells of the second and third quartettes.
They become thickly covered with somewhat small cilia. The three

PODAXONIA

375

intermediate cells of the Molluscan cross la122, lb122, lc12'2, also
acquire cilia and are incorporated in the prototrochal girdle. They
are the secondary trochoblasts (Fig. 303). Of the fourth quartette
of micromeres 4d is formed long before the others, and, as usual,
immediately divides into right and left sisters 4dr and 4cl', which are
the mother cells of the mesoderm. The residual macromeres
eventually form a plate of endoderm which is situated beneath the
" b " arm of the Molluscau cross.

As in Patella and Dcntalium the process of gastrulation begins
by the sinking-in of this plate, and this in-sinking is caused by a

dc

end.

•slom

FIG. 304. — Nearly sagittal section of an embryo of Phascolosmm/ rufgare at the
stage when gastrulation is beginning. (After Gerould.)

a.p, apical plate; il.c, dorsal cord ; end, endodermal cells derived from residual macronirrrs ; / //«/ i,
accessory endodermal cells, derived from the mesodermal band ; h.fi, head-blastema ; mcs, mesoderinal
band; p.tr, prototrochal cells; st.om, cells which give rise to the stoinudaruni ; t.li, culls formm;,' the
trunk-blastema.

change of shape in its component cells. These elongate and become
flask-shaped, the bulb of each flask passes into the segmentation-
cavity or blastocoele whilst the neck remains for a time connected
with the surface (Fig. 304).

Further divisions at the upper pole of the egg result in the pro-
duction of a diamond-shaped apical plate of cells surrounding four
central cells, the apical cells, which acquire long stiff hairs and form
the apical sense-organ. The cells surrounding this apical plate then
begin to sink inwards so as to form a ring-shaped imagination which
is, as a matter of fact, the head-blastema. The trunk-blastema lies
on the ventral surface, behind where the blastopore is situated and

376 INVEKTEBRATA CHAP.

where the stomodaeum is eventually formed. It is a triangular
plate of cells with the apex directed forwards and is formed of
descendants of 2d. Trunk-blastema and head-blastema are con-
nected in the mid-dorsal line by a narrow cord of cells — tbe dorsal
cord (d.c. Fig. 304).

The mother cells of the mesoderm, by this time, have each given
rise to an anterior band of four cells and to a minute posterior cell,
which lies against the endoderm, and which, as in Mollusca, probably
gives rise to the intestine. The closure of the blastopore is effected
partly by the forward growth of the trunk-blastema and partly by
the in-sinking of the descendants of 2a, 2b, and 2c which give
rise to the stomodaeum.

The embryo becomes a larva by beginning to swim. This
happens about twenty-four hours after fertilization of the egg. The
larva does not burst the egg-membrane, but carries it about with it.

The prototroch, composed of the primary and secondary trocho-
blasts, is a broad belt of cells covered with minute cilia. There, is a
well-marked metatroch consisting of a girdle of long cilia. Between
prototroch and metatroch is situated the opening of the stomodaeum,
which is surrounded by a special girdle of small cilia. In front of
the apical plate, to the right and left of the middle line, eye-spots
are found (oc, Fig. 305); these are situated just above the region
where the cells are being invaginated to form the head-blastema.

Until thirty-six hours after fertilization have elapsed, the larva
remains spherical. After that time the posterior portion of the
body elongates more rapidly than the anterior portion, and at the
beginning of the third day, in the case, at any rate, of Phascolosoma
vulgare, it sinks to the bottom. At this period the egg-membrane is
at last shed, and underneath it a fine cuticle is now to be seen, which
has been mistaken for the persisting egg-membrane but is in reality
quite distinct from it.

Before, however, this happens, very considerable changes occur in
the Trochophore larva. The appearance of the apical plate changes,
since the sense-organ appears to move to its anterior edge ; this is
due to the anterior part of the plate becoming iuvaginated to form the
cerebral ganglion. Hound the edge of the apical plate is found the
prae-oral band of cilia ; this has nothing to do with the prototroch,
the cells composing which carry quite minute cilia. Behind the proto-
troch there is a narrow band of ectoderm from which the mesecto-
derm is formed; that is to say, from this band cells are budded inwards
into the blastocoele. Some of these cells are transformed into
longitudinal accessory retractors (ret.aec, Fig. 306), others become
changed into circular muscles. The principal retractors are formed
from the cells of the apical plate which bear the prae-oral circle of
cilia. These retractors retain throughout life their insertion into the
ectoderm at the point where they originated from the apical plate
(ret.d, ret.v, Fig. 306).

Before the Trochophore larva sinks to the bottom the rudiment

X

PODAXONIA

377

of the ventral nerve cord makes its appearance as au unpaired ecto-
dermic thickening. This thickening becomes detached from the
ectoderm and sinks inwards, and in Phascolosoma youldii (but not
iu Phascolosoma vulgare~) it becomes divided into two to four segments.
These may be regarded as ganglia of the nerve cord. In Phasc,oloxuiii«
gouldii the mesoderm also becomes divided into segments (men1, mes2,
mes3, Fig. 306). The anus is formed, about the forty-fifth hour, by a
narrow cone of endoderm cells growing out dorsally and becoming

mlr

•h.

FIG. 305. — A Trochophore larva of P/iavcolosoinn ruli/nre a little niorr tlian thirty-six
hours old. (After two figures by Gerould combined. )

'il>, apical plate with its tuft of cilia ; eh, chorion still investing the embryo ; hJi, heafl-blastnna ;
mlr, rnetatroch ; ii.tr, prototrocli ; oc, eye-spots; »tnni, stomodaeum ; t.li, trunk-blastema.

attached to a cluster of ectoderm cells which become slightly invagin-
ated. Somewhat later the coelomic cavity appears ; in Pkasco/omninr
gouldii spaces appear in each of the mesodermal segments, which fuse
together and form one undivided cavity. In P. riili/iire, however, in
which the mesoderm is unsegmented, the coelom a]»p(iars from the
beginning as an undivided space.

When the Trochophore sinks to the bottom the prototroch is got
rid of by a most peculiar process. The inner ends of the large cells
of which it is constituted break down into yolky granules ; these

378

INVERTEBRATA

CHAP.

(y.g, Fig. 306) are shed into the coelom aud are there taken up by
amoebocytes and absorbed. In this way, gradually, the whole of
the prototroch is disposed of. During this process the larva takes
011 a cylindrical form with a diminishing ring-shaped swelling in
front ; this swelling is the disappearing prototroch.

A nerve strand runs from the cerebral ganglion to the apical
sense-organ, and from this ganglion originate a pair of muscle cells

mes
ect

end-

mfr

-UllC

coe

FIG. 306. — Nearly sagittal sections through metamorphosing trochophores of
A, sagittal section to one side of the middle line of the larva of Phasi-iil
about fifty-seven hours old, to show the segments of the mesodermal band. (After two
figures by Gerould combined. ) B, sagittal section nearly median of the larva of J'has-
colosoma vulgare, about forty-eight hours old. (After Gerould.)

a, anus; ap, "apical plate; cue, coclomic cavity; end, endodermie tube; mes1, wics2, wcs-'; segments
of tin1 mesodennic band ; mes.ect, point of origin of the mesectodenn ; rn.tr, mrtatrnrli ; n.nijl, nerve
collar ; jir.c, prae-oral circle of cilia ; ]/ti-, degenerate yrototrochal cells ; -ret.nr.c, accessory retractors ;
n<t.d, ilursul retractor muscles formed from ectoderm; ret.p, ventral retractor muscles formed from
rHudrrm ; s.o.g, supra-oesophageal ganglion ; stum, stoinodarnm ; c. ».<•, ventral nrrve coi-d ; y.g, yolk-
granules, remains of prototrochal cells.

which run backwards and are inserted into the dorso-lateral region
of the skin behind the prototroch. At the sides of the ventral
nerve plate there are situated two series of clusters of muscle cells.
The more ventral of these run backwards towards the posterior
insertion of the retractors ; the more dorsal extend forwards to the
region between prototroch and post-oral circlet.

The invagination of the anterior region of the body, so as to form

PODAXONIA

379

an introvert, is begun as soon as the coelomic cavity appears in the
niesodermic bands. Then the retractor muscles, whose formation
was described above, begin to act and to pull in the whole apical

region.

Up till the end of the sixth day there is a freely projecting
flattened prostomium, ciliated on its under surface. In the second
week this prostomium grows out into a dorse-lateral extension 011
each side, on which ciliated tentacles are developed. Beneath the
mouth a ciliated under-lip is formed.

-pre

reU

FIG. 307. — Youug specimens of
1'hii.wilosoma youltUi after the
metamorphosis. (After Gerould.)

A, young worm six and a half days
did. L5, young worm thirty days old.
Letters as in preceding figure. In ad-
dition: He/ i/i, nephridium ; ten, ridge-like
outgrowth of prostomium, on which
ciliated tentacles of the adult appear.

>rc

retv

Both species of Phascolosoma then develop a circle of hooks round
the base of the introvert ; these can still be made out as minute
hooks in the adult P. rulrjare, but in P. gouldii they entirely dis-
appear. The papillae, so characteristic of the adult skin, appear as
oval clusters of ectoderm cells which project slightly inwards towards
the coelom.

Large yellow cells (ehloragogen cells) are disposed in lines alnn-
the coelom. The two nephridia (neph, Fig. 307) appear to originate
as solid ectodermal ingrowths, in each of which a cavity appears later.
They come to open into the coelom by the intervention of cells of

380 INVERTEBKATA CHAP.

coelomic origin, from which the internal funnel or nephrostome is
formed.

As the body grows longer and longer the anus appears to move
forwards, but this appearance is simply due to the fact that the part
of the body intervening between the apical plate and the anus does
not grow nearly so fast as tbe portion situated behind the mouth,
on the ventral surface; this disparity of t/roivth is the essential
characteristic of all Podaxonia.

If we review the development which has just been described, we
shall find ourselves driven to the conclusion that, not only are
Phascolosoma and its allies descended from the common Ctenoph ore-
like ancestor of Annelida and Mollusca, but that they have diverged
from the Annelid stem after the beginnings of segmentation had been
acquired, and that they represent one mode in which the descendants
of the primitive Annelida were adapted to a burrowing life.

SIPUNCULUS

The development of the well-known Mediterranean genus
Xipunculus has also been worked out by Hatschek (1883) though
not at all in the same detail as Gerould has worked out Phascolosoma.
It agrees in all essentials of its embryonic and larval history with
Phascolosoma, the chief differences being the form which the proto-
troch assumes and the mode of disposing of it.

In Sipunculus the prototroch, instead of being represented by
sixteen primary prototrochal cells, is represented by a broad mantle
of comparatively small cells carrying short cilia. This mantle is,
however, incomplete in tbe mid-dorsal line, where a narrow line of
sunken cells connects the head- and trunk-blastema. This line of
cells corresponds to the dorsal cord of Phascolosoma. When the
larva metamorphoses the whole of the mantle is cast off, as in Nucvla
amongst Mollusca, and is not absorbed into the coelom as in
Phascolosoma.

PHORONIDEA

A form of great interest, which was placed in the old group of
Gephyrea under the division Gephyrea tubicola, is Phoronis.
Phoronis is now made the type of a special family, the Phoronidea,
which Lankester considers to belong to the Polyzoa, but which we
regard as more nearly related to the Sipunculoidea whose develop-
ment we have just discussed.

Phoronis agrees with the typical Podaxonia in tbe ventral
development of the body, but instead of living in sand and mud it
inhabits a, leathery tube which it secretes for itself. It possesses, like
most Podaxonia, a curved lateral extension of the lips of the mouth
bearing ciliated tentacles, but these, instead of being prae-oral as in
Phascolosoma, are post-oral.

PODAXONIA

381

The full embryonic history of Phoronis has not been satisfactorily
made out, although a preliminary account of the subject has been
given by Caldwell (1883 and 1885), and further work on the subject
has been done by Masterman (1898), Ikeda (1901), de Selys Long-
champs (1902), ami Shearer (1900).

The free-swimming larva of Plioronis is termed Actinotrocha,
and was regarded as an independent organism before its lii'e-histoiy
was known. Its remarkable metamorphosis into the adult form was
described by Metschnikoff (1871), while a minute description of 1.1 ir
structure of the adult larva was
given by Goodrich (1905).

Mastermau's paper awakened
widespread interest and created
a lively controversy. He en-
deavoured to show that Actiuo-
trocha, like the larva of Bctlano-
glossus (p. 575), possessed five
coelomic sacs, viz. a prae-oral
and two pairs of lateral sacs ; and
that these sacs were developed
as outgrowths from the gut,
and that consequently Phoronis
was allied to the Protochordata,
and in particular to Ceplia-
lodiscus, which has ciliated
tentacles like those of the
Actinotrocha larva. He even
endeavoured to find the homo-
logue of the notochord in two
glandular pouches which project
forwards from the stomach of
Actinotrocha (gl, Fig. 311).

The Actiuotrocha larva
possesses a hood-shaped prae-oral
lobe covered with minute cilia and carrying a thickened apical plate.
Somewhat below the centre of its upper surface the prae-oral lobe
contains a cavity, called by Masterman the prae-oral coelom.
Behind the mouth there is an oblique ciliated baud, in other words
a metatroch, which is drawn out into a series of hollow tentacles
(Fig. 309). The tentacles contain cavities which open into right and
left loop-shaped vessels, situated at the sides of the oesophagus, which
were compared by Masterman to the "collar coelomic cavities" of
Cejihalodiscus. There are a pair of nephridial tubes which, according
to Masterman, open internally into the collar -cavities and are
compared by him to the collar pores of Ce-'plmlodixcus. Behind
these a pair of coelomic sacs flank the, alimentary canal, which
correspond to the trunk coelomic cavities of Cephalodiscus. A
ciliated girdle or telotroch encircles the hinder end of I lie larva.

FIG. 308. — Lateral view of the Actinotroclia
larva of /'lionnu's. (After Metschnikoff.)

KII, apical plate ; li.r, blood-vrssrl ; in, mouth ;
in.tr, nirtatroeh ; t./r, telotrorli.

382

INVERTEBRATA

CHAP.

Unfortunately Masteruiau's fascinating hypothesis has not been
sustained by subsequent workers. Thus, Goodrich shows clearly that
the so-called prae-oral coelom is merely a portion of the blastocoele,
or primary body-cavity, corresponding to the cavity surrounding the
gut in a Trochophore larva ; and that the nephridia cannot bo homo-
logous with collar pores, because they end blindly internally and are
beset with solenocytes projecting into the blastocoele ; they are in
fact archiuephridia like those of Annelida. Goodrich admits the
existence of collar and trunk coelomic cavities, but Ikeda, de Selys

Longchamps, and Shearer
deny that these arise as endo-
derinic diverticula.

In justice to Masterman

n.p
oes

it ought to be noted that

arch

TJlCi

mes

FIG. 309. — Diagrammatic frontal section of the
Actinotrocha larva of Phomnis (spl) captured
near Ceylon. (After Goodrich.)

np, apical plate ; col.c, collar coelom ; int, intestine ;
mtf, tentacles of the metatroch ; ncph, nephriilium ;
oes, oesophagus ; pr.bs, prae-oral blood space ; s.n.p,
subnenral pit; so?, solenocytes of the nephridia; >/,
stomach ; tr.i; trunk coelom ; t.tr, telotroch.

FIG. 310. — Longitudinal hori-
zontal section of the einliryo
of an Australian species of
Phoronis. (After Caldwell.)

ivrrli, arclienteron ; mcli, mesen-
chyme cells ; mes, divcrticnla of the
archenteron giving rise to the meso-
derm of the trunk-cavities according
to Caldwell. According to Shearer,
an ectodermic pit giving rise to the
tubes of the two nephridia.

Caldwell described the coelom as arising from two posterior outgrowths
from the gut (Fig. 310) ; and though Shearer asserts that the bilobed
ingrowth seen by Caldwell is an ectodermic pocket which gives rise
to the tubes of the nephridia, yet the fact that the first trace of the
coelom seen by him was an impaired bilobed sac, lying close to the
dorsal surface of the hinder end of the gut, renders it possible that after
all Caldwell and Masterman are right and that the trunk coeioni does
arise as a pair of posterior diverticula of the gut, at least in some species.
Further work is needed to obtain complete certainty on this point.

x PODAXONIA 383

Iii any case, however, we fear that Masterman's hypothesis cannot
be upheld. Even if the " trunk " coeloin does arise in the way which
lit- describes, this does not necessarily prove a close affinity between
P/toi'onis and the Protochordata, because we have already seen that
the origin of the niesoderm from 4d in Annelidau eggs must be
regarded as a modification of such a mode of development, and
Erlanger has actually described the rnesoderm as arising as a pouch
in Paludina.

The fatal flaw in Masterman's theory is the absence of a prae-oral
coeloin in the Actinotrocha larva, and though it is conceivable that
the uotochord of CepJialodiscus should be represented by a paired
structure in Actinotrocha, yet the glandular pouches of Actinotrocha
have no resemblance to a notochord. The notochord in all Proto-
chordata, and in Vertebrata, is a modification of the endoderm into
a supporting tissue, by an increase in thickness of the cell-walls of
its component cells and the degeneracy of their contained protoplasm.
Such a change can be seen in the endoderm of the solid tentacles
of the hydroids of Tubularia, for instance, as compared with the
endoderm of the hollow tentacles of Hydra. But the mere fact that
the cells composing these glandular pockets in Actinotrocha contain
large vacuoles, does not create any special resemblance to a notochord.

On the whole, the early development, so far as it is known,
creates the impression of being a modified form of the development
described for Phascolosoma. In both forms the nephridia arise as
ectodermal pockets which, subsequently, after the metamorphosis
has been accomplished, acquire openings into the coelom. The ciliated
prae-oral lobe of Phoronis may be compared to the prototroch of
Phascolosoma,. In both forms the metatroch is prominent.

After the Actinotrocha has led a free - swimming existence for
some time, and has increased in size, an invagination of the ectoderm
appears on the ventral surface, mid-way between mouth and anus.
This pouch increases in depth until it reaches the intestine of the
larva, to which it becomes adherent. The intestine increases greatly
in length and is thrown into several loops (Fig. 311) ; the pouch is
also thrown into folds as it grows longer.

At length a critical point of growth is reached, at which meta-
morphosis suddenly supervenes. The ectodermic sac is everted and
forms a huge evagination which constitutes the main part of the
body of the " worm." As the intestine was attached to the apex of
this sac, when this is evaginated the intestine is drawn out in a U
shape. The ciliated tentacles of the post-oral band fall off, but
from their bases grow out stumps from which the adult tentacles are
later developed. The prae-oral lobe disappears, according to Caldwell
(1883) it is bodily amputated and falls into the gaping mouth and
is there digested. The whole metamorphosis occupies only a quarter
of an hour. We ourselves can testify that on one occasion we left
an advanced Actinotrocha in a watch-glass, left the room for a short
time, and on coming back found a young Phoronis.

384

INVEKTEBRATA

CHAP.

If Caldwell lias given the details of the metamorphosis correctly
it is exceedingly ditiicult to interpret, for his account would seem
to imply that the apical plate and subjacent ganglion are sacrificed,
in which case the cerebral ganglion of the adult must be a new

B

ate.n

uw

tr

FH;. 311. — Three stages in the meta-
morphosis of the Aetinotrodiu
larva of Phoronis, seen from the
side. (After MetschnikofF. )

A, stage in which the ventral ecto-
dfrmic imagination has just made its
appeal ance. B, stage in which the ventral
invagination is partly everted. (', stage
in which the metamorphosis is almost
complete. a.ti'ii, rudiments of adult
tentacles; i/l, glandular pocket of the
stomach regarded by Masterman as a
homologuo of the notochord ; int., intes-
tine ; in i', ectodermic invagination which
becomes everted to form the body of
the worm ; l.ten, larval tentacles of the
metatroch ; pr.l, prae-oral lobe ; si,
stomach ; t.tr, telotroch.

formation. Now in the metamorphosis of every Trochophore so far
studied, the apical plate and the associated ganglion form the head-
blastema, and persist through larval life into the adult condition.
It is possible that Caldwell has made a mistake in this matter, and
that it is the hood in front of the ganglion, which we have already
compared to a broad 'prototroch bearing minute cilia, which is

x PODAXONIA 385

amputated ; and that this proceeding is equivalent to the casting off
or absorption of the prototroch in other forms.

If this supposition be justified, then the rest of the metamorphosis
can be viewed as a modification of the process of gradual growth
of the ventral part of the body, already observed in Phascolosoma
and Sipunculus. It is a very instructive modification, showing the
kind of secondary change which may be expected to occur in ontogeny.
It is another example of the complete omission of the intermediate
stage of development between the Trochophore stage and the adult
condition. This intermediate stage must have existed in the history
of the race and doubtless occurred at one time in the history of the
individual.

The general conclusion then, to which we are led by a review of
the development of Phoronis, is that it really does belong to the
group of Sipunculus and Phascolosoma, and that the classification of
the older authors is so far justified. This conclusion, however, raises
another series of most interesting questions. The structure of
Phoronis is so similar to that of the Phylactolaematous Polyzoa
that Laukester (1890) regarded Phoronis as a Polyzoan ; and it seems
difficult to evade this conclusion. But in that case Phoronis would
be the only solitary Polyzoan known, and all the true Polyzoa
(leaving out of account the anomalous Eutoprocta) must be regarded
as modified Podaxonia.

LITERATURE CONSULTED

Caldwell, W. H. Preliminary Note on the Structure, Development, and Affinities
of Phoronis. Proc. Roy. Soc. (Lond. ), vol. 34, 1883.

Caldwell, W. H. Blastopore, Mesodenn, and Metameric Segmentation. Quart. Journ.
Mic. Sci., vol. 25, 1885.

Gerould, J. H. Studies on the Embryology of the Sipunculoidea, I. The Embryonic
Envelope and its Homologue. Mark Anniversary Volume, 1903.

Gerould, J. H. Studies on the Embryology of the Sipunculoidea, II. The
Development of Phoscolosoma. Zool. Jahrb. (Anat. u. Out.), vol. 23, 1907.

Goodrich, E. On the Body - cavities and Nephriclia of the Actinotrocha Larva.
Quart. Journ. Mic. Sci., vol. 46, 1903.

Hatschek. Uber die Entwieklung von Sipunculus nudus. Arb. Zool. lust. Wim,
vol. 5, 1883.

Ikeda. Observations on the Development, Structure, and Metamorphosis of
Actinotrocha. Journ. Coll. Sei. Imp. Univ., Tokyo, vol. 13, 1901.

Lankester, E. R. Zoological Articles "Polyzoa," repub. from Encycl.
Britt,, 1890.

Masterman. On the Diplochorda, Parts I. and II.' Quart. Journ. Mic. Sci., vol.
40, 1897 ; Part III., ibid. vol. 43, 1900.

Metschnikoff, El. Uber die Metamorphose einiger Seetiere, III. Actinotrocha.
Zeit. AViss. Zool., vol. 21, 1871.

de Selys-Longcbamps. Recherches sur le developpement de Phoronis. Arch, dc
biol., vol. IS, 1902.

Shearer-Cresswell. Studies on the Development of Larval Nephridia (I. Phoroni , .
Mitt. Zool. St. Neapel, vol. 17, 1906.

VOL. I 2 C

CHAPTER XI
POLYZOA

Classification adopted —

Phylactolaemata

Polyzoa Ectoprocta , | Cydostomata

Gymnolaemata - Ctenostomata

[Cheilostomata
Polyzoa Entoprocta

THE group of the small colonial animals known as the Polyzoa
includes two divisions, known respectively as the Ectoprocta and
the Entoprocta, about whose affinity with one another there is very
considerable doubt. Both groups agree in being colonial, in possessing
a ring of ciliated tentacles surrounding the mouth, by the action of
which they obtain their food, and in having the principal nerve
ganglion situated between mouth and anus on the surface which is
normally turned upwards.

In the Ectoprocta the coelom is spacious and well developed,
and from its walls the genital cells are developed ; whilst the body
is divided into a posterior part (the zooeciurn) and an anterior introvert
(the polypide). The ring of ciliated tentacles surrounds the mouth
alone, and is therefore morphologically a metatroch. In all these
features the Polyzoa Ectoprocta resemble the Podaxonia.

In the Entoprocta, on the other hand, the coeloin is entirely
suppressed, except in so far as it is represented by the minute
cavities of the genital organs. There are distinct nephridia, ending
internally in blind ciliated ends ; the body is divided into an upper
cup -like part called the calyx, and a lower solid stalk. The ring
of ciliated tentacles surrounds both mouth and anus, and is, morpho-
logically, a prae-oral band or prototroch.

Prouho (1892), Harmer (1896), Seeliger (1906), and Czwiklitzer
(1909) regard the two groups as closely allied, but Korschelt and Heider
(1892) regard them as totally distinct phyla. We shall deal with them
separately in this chapter, and, after having studied both, indicate
our opinion as to which side in this controversy has the greater weight
of evidence in its favour. We begin with the Polyzoa Ectoprocta.

386

CHAP, xi POLYZOA 387

POLYZOA ECTOPKOCTA

In the vast majority of Polyzoa Ectoprocta the egg is fertilized
whilst it is still iu the maternal tissues, and undergoes the first
stages of its development there. It finally emerges as a free-
swimming larva, with more or less degenerate gut, and, after a short
tree existence, fixes itself and grows into the first person of the future
colony. In a few cases, however, the eggs are shed into the sea and
are fertilized there, and a comparatively long larval development
ensues ; this type of larva has a well-developed gut, and can feed itself.
In these latter cases we have obviously the primitive type of Ecto-
proctan development, and it is they which deserve our closest attention.
They have been most carefully studied by Prouho (1892), and we
select for special description one of the forms described by him which
has a long larval development.

MEMBRANIPOEA PILOSA

Membranipora pilosa is a species occurring abundantly around
the coasts of Europe as a delicate lace-like incrustation on the fronds
of Laminaria. Closely allied species are found in similar situations
all over the world. Mevibranipora is easily kept living iu vessels
of clean sea-water ; the eggs are freely discharged, and develop into
the young free -swimming larva, which is termed Cyphonautes, a
name bestowed on it when it was supposed to be an independent
organism. Its true nature was shown by Schneider (1869), who
captured it in the sea and watched it metamorphose into Membrani-
pora. To rear Cyphouautes in captivity up to this stage would
require arrangements for feeding it with diatoms such as have been
employed with success in the case of many other larvae.

If the vessels in which the larvae are kept have been previously
coated with a layer of transparent photoxyliu, then, when the larvae
fix themselves, they can be removed from the sides of the vessel
together with the photoxyliu to which they are adherent, and cut
into sections. Kupelwieser (1905), to whom we owe this method,
has given us the best account of the metamorphosis of the larva.
He paralysed the free-swimming larvae by adding drops of hydro-
chlorate of cocaine to the sea- water in which they were swimming ;
the larvae were then preserved in Flemming's fluid or a mixture
<;f the solution of corrosive sublimate and glacial acetic acid.

In the development of the egg of Memlranipora the division
into blastomeres takes place in an absolutely even and regular
manner, and recalls in a good many ways the segmentation of the
egg of Poiijgordius. At the 16-cell stage all the blastomeres are
equal to one another in size ; the embryo, however, does not form a
sphere, but a biconvex lens (Fig. 312), the axis joining the animal
and vegetable poles being very much shortened. The blastocoele is
excessively narrow. At the 32-cell stage the flattening is still more

388

INVERTEBRATA

CHAP.

marked, and four blastomeres situated in the centre of one face are
distinguishable by their granular contents. These blastomeres are
the rudiment of the endoderm, and the blastula stage may be said
to be now completely attained.

At the next stage the endodermal cells sink inwards, filling up
the blastocoele, whilst the other cells meet beneath them, and so the
gastrula is formed. One is thus reminded forcibly of the extreme
flattening which the blastula of Polygordius undergoes just prior to
gastrulation. The blastopore, or aperture left by the in-sinking of
the endoderm cells, is almost immediately closed. The face on which
it was situated will be called the oral face.

Two cells, placed symmetrically to the right and to the left of
the middle line, are found at the next stage in the development of
Alcyonidium albidum, which also gives rise to a Cyphonautes-like
larva ; but they have not as yet been observed in the case of

end

FIG. 312. — Early stages in the development of the egg of Membranipom

(After Prouho.)

A, stage of sixteen blastomeres seen from the side. B, stage of thirty-two blastomeres seen from the
underside. C, gastrula seen from the side, blji, blastopore ; end, cells which form the endoderm.

Membranipora, though it is quite probable that they exist there
also. In the case of Alcyonidium they help to form larval muscles,
which traverse the blastocoele, and these muscles also exist in the
larva of Membranipora. These two cells, whose exact origin Prouho
could not determine, he calls the mother cells of the mesoderin.
They are, however, situated in front of the mass of endoderm, and
have, in all probability, nothing whatever to do with the true pole
cells of the mesoderin in Polygordius which give rise to the coelomic
wall, but are rather to be compared to the mesectoderm of Polygordius,
i.e. cells derived from the second quartette of micromeres, i.e. from
the ectoderm which gives rise to the blastocoelic muscles in the larva.
Coming now to the next changes observed in the embryo of
Meiribranipora, we find that the whole embryo takes on a conical
shape, the oral face forming the base of the cone, whilst at the upper
end, where the point of the cone should be, a thickening of the ecto-
derm becomes visible, which is termed the apical organ and which
is homologous with the apical plate of Annelidau and Molluscan
larvae. On the oral face now appears a wide depression. This is

XI

TOLYZOA

389

the beginning of the enormous stomodaeum which pushes

the

endodermic mass towards the posterior end of the embryo.

The embryo now adheres by its oral face, and also by the apical
organ, to the vitelline membrane, and at the same time it alters its
shape, so that it becomes compressed from side to side. The vitelline
membrane seems to be absorbed where it is in contact with the
embryo; stiff cilia or sense-hairs appear on the apical organ, and

mes

proct

stem

FIG. 313. — The development of the larva of Membranipora pilosa. (After Proulio. )

A, young larva .just free from the egg-membrane ; end, solid mass of cells which will be hollowed
out to form the stomach. The stomodaeum is formed, but does not join the stomach as yet. B,
young larva in which the stomodaeum lias joined the stomach. C, larva a little older than that repre-
sented in B, in which the proctodaeal invagination has been formed, ap, apical plate ; co, corona ;
proct, proctodaeal invagination ; mes, ectomesoderm.

powerful locomotor cilia on certain cells of the thickened ridge
of ectoderm, termed the mantle, which forms the border of the oral
face. The space surrounded by the mantle has become concave, and
it is termed the atrium ; into it the stomodaeum opens. The
of ciliated cells is termed the corona.

The embryo now becomes a larva and swims about ; the remnants
of the vitelline membrane which still envelop it in the middle are
brushed off. After the free life lias begun the mass of cells forming
the eudoderm becomes hollowed out and forms the larval stomach.

ring

390 INVEETEBEATA CHAP.

Mesoderni cells in front of this multiply and form a string leading
from the aboral thickening to the ventral surface ; this string is the
rudiment of the main dorsal muscle of the larva. Shortly afterwards
an ectodermic invagination is formed in the posterior part of the oral
face. This is the proctodaeum, the rudiment of the anus and of the
larval intestine. It grows in length and joins the stomach, and the
latter opens into the stomodaeum, in which cilia become developed,
and so the definite alimentary canal is completed and feeding begins.
A delicate bivalve shell is secreted by the larva ; each valve is tri-
angular, and the apical organ protrudes between the apices of the
valves, whilst their bases flank the corona.

Soon afterwards the ring of ciliated ectoderm which we have
termed the corona, and which we may compare to the prototroch of
the Trochophore larva, begins to exhibit modifications. In front of
the mouth a pair of transverse ridges grow inwards from, it at right
angles to its course, and constitute a transverse band of cilia across
the ventral face of the larva. A pair of similar ridges also grow in-
wards from the oral band in front of the anus, and constitute a
second transverse band of ciliated ectoderm there.

When the Cyphonautes is fully grown it possesses two other
organs : a so-called " piriform organ " in front of the mouth, con-
sisting of columnar ectoderm cells, and an "internal sac," which
is an invagination of the ectoderm between mouth and anus. The
" piriform " organ arises as an ectodermal invagination, which becomes
almost shut off from the exterior, but remains connected therewith
by a narrow longitudinal slit, the cells lining which are covered by
powerful cilia. This slit is termed the vibratile cleft (v.cl, Fig. 314).
Though these ciliated cells afterwards meet those of the corona they
originate quite independently of it, and only subsequently come into
contact with it. The cells of the piriform organ itself take on a
glandular appearance, and emit a secretion into its cavity. The
main muscle, alluded to above, leads from the apex and sides of the
piriform body to the apical organ, and then passes beneath this to
run down the posterior aspect of the larva to the most posterior cells
of the corona.

In front of the ciliated groove which forms the opening into the
piriform organ there is a rounded ciliated pit which is delimited from
the groove by a blunt prominence. On the hinder aspect of this pit
there is a small group of cells which carry exceptionally long cilia-
cilia which, moreover, are bent in a peculiar hook-like manner, and
which swing backwards and forwards in the middle line. These are
termed the vibratile plume. A special branch of the main dorsal
muscle pierces the glandular sac of the piriform organ and continues
its course to end at the base of the cells carrying this special " vibratile
plume." A strand of nerve fibres accompanies this muscular strand.
But the main mass of the muscle and nerve proceed downwards,
and whilst the nerve fibres become more numerous the muscle fibres
decrease in number. Many of the nerve fibres go to the ciliated cells

POLYZOA

391

of the vibratile cleft, but after these have been given off the main
mass of the nerve fibres proceeds to the ciliated cells of the prototroch
Muscle fibres also go to the cells of the vibratile cleft,

or corona.

mused

st~

al

CO

vcl

musclalp

FIG. 314. — Median sagittal section of the fully grown Cyphonantes larva of Membmnipora
pilosa on the top of which have been traced certain structures (muscle fibres and corona,
etc.) lying to the right of the median plane. (After Kupelwieser, slightly altered.)

.-li'iM, main adductor muscle of the valves ; Add'2, accessory adductor muscle of the valves ; r'/<.;/,
cells of the apical plate of the ganglionic nature ; a]>.r/l, cells of the apical plate of a glandular nature ;
ii/i.ris, cells of the apical plate of a visual nature ; cil, cells forming anterior and posterior borders of
the larva carrying long cilia ; col, anterior section of the corona ; co2, posterior section of the corona ;
<//•.<•, granular cells; Is, internal sac; int, intestine; m.e, mucous cells of mantle edge; wusr.circ.oes,
circular muscles surrounding the oesophagus ; mvw.il, dorsal muscle ; musc.dl, branch of dorsal muscle
which is inserted in the apical organ ; mnsr.d", branch of dorsal muscle which curves back under the
apical organ and is inserted in the posterior section of the corona ; musc.lat.it, anterior part of lateral
muscle ; miisi'-.lnt.ti, posterior part of lateral muscle ; musc.sk, sucker muscle ; ?(./, nerve lilires leading
from apical organ to vibratile plume and to corona; ncs, oesophagus; y>.n, piriforrn organ; sec,
secretion produced by the cells of the internal sac ; i'.d, vibratile cleft ; v.)>J, vibratile phnne.

and to the cells of the corona, but in addition muscle fibres are given
off which are inserted in the upper part of the piriform organ, and
others which encircle it after the manner of circular fibres.

Kupelwieser regards the function of the piriform organ as skeletal,

392 INVEKTEBBATA CHAP.

that is to- say, he thinks that it affords a convenient insertion for
muscle fibres ; those inserted in its upper part he regards as retractors,
the encircling fibres as protractors, and the vibratile plume he con-
siders the real sense-organ. He believes that this sense-organ comes
into play just before the fixed life is taken up, and that its function
is to select a suitable spot for the fixation of the larva.

The internal sac, or sucker, arises just in front of the anus, and,
according to Kupelwieser, it begins as a solid thickening of the
ectoderm, which soon splits into two layers separated by a cavity.
Prouho, however, says that it arises as an invagination just in front
of the anus. This little sac develops, as larval life proceeds, into a
wide, spacious sac, which is drawn out into two horns. The upper
wall of the sac remains thin, but its lower wall, where it abubs 011
the atrial cavity, becomes glandular, and produces great masses of a
slimy secretion. Eventually this wall breaks down and allows the
sucker to open into the atrial cavity, into which the secretion is then
discharged. Two muscles arise, one on each side, from the ectoderm
of the central parts of the flat sides of the larva, and are inserted
into the upper wall of the sac. These muscles, termed the sucker
muscles, only come into play at the metamorphosis.

The ectoderm of the sides of the larva, as we have already noted,
secretes two thin valves of shelly material, which thus form a
bivalve shell protecting the larva. Bound the edges of each triangular
shell-bearing area there runs a cushion of large swollen cells, filled
with a mucoid secretion, thus taking on the outline of a triangle.
From the base of this triangle a ridge of the same material projects
upwards a short distance. The ectoderm covering the narrow sides
of the larva, between the valves, is covered with short cubical ciliated
cells.

From this description it follows that the apical organ is bounded
laterally by the cell-cushions, and front and back by cubical epithelium.
The apical organ itself is a two-layered, slightly concave plate, or
shallow cup of cells. The rim of this plate is composed of converging
columnar cells, each bearing a single stiff cilium or sense -hair.
Inside this outer ring comes a second ring of cells bearing pigment,
to which Kupelwieser assigns a visual function, while in the centre
there is a mass of clear rounded cells. From the fact that a bundle
of nerve fibres proceeds from these inner cells, Kupelwieser draws
the conclusion that they are of a ganglionic nature.

The fibres of the dorsal muscle penetrate between the cells of the
apical organ in order to attain their insertion ; but not all the fibres
of the dorsal muscle, in fact only the minority, have this insertion.
The majority of the fibres of the dorsal muscle pass back under the
apical organ and diverge into bundles, right and left, and are inserted
into the ciliated cells of the posterior part of the corona. Most of
the fibres belonging to the dorsal muscle are striated, but some
muscles have smooth fibres.

There is an adductor muscle connecting the two valves of the shell

xi POLYZOA 393

beneath the stomach, and above it there is a similar smaller muscle,

the accessory adductor. Two lateral muscles, an anterior ami
posterior, arise on each side from the same area of the shell \\liic-h

394 INVERTEBKATA CHAP.

gives rise to the sucker muscles, and are inserted in the cells of the
corona.

During its active life the larva swims with its apical organ
directed forwards; but when the free life draws to an end it glides
over the bottom, with its oral surface directed downwards, and during
this period the vibratile plume can be seen to carry out tactile move-
ments. Finally, the sucker is everted and forms a thin flat plate of
cells which adheres to the substratum (Fig. 315). All the muscles
except the sucker muscles contract strongly, and the piriform and
apical organs are in consequence strongly retracted. The outer edges
of the adhesive sucker turn upwards and unite with the edges of the
mantle, and the remnant of the atrial cavity is converted into a
ring-shaped space, towards the inner side of which the cilia are
directed. Then the muscles connecting the sucker with the valves
of the shell contract, and with great strength, so that the valves of
the shell are, so to speak, flattened out over the compressed larva.

Histolysis of the larval tissues now begins. First the cushion
cells disintegrate and their mucoid contents are cast into the ring-
shaped atrium. In this way the ciliated cells of the corona become
cut loose from the mantle edge, the cells of which join the edge of
the adhesive plate formed from the sucker ; and the remnants of
the coronal cells are found floating in the ring-shaped atrial cavity.
The apical organ is very deeply invaginated and broken loose from
the flanking cushion cells ; the adjacent ordinary ectoderm cells
meet above it, and from it, afterwards, the polypide of the first bud,
i.e. the alimentary canal and ciliated tentacles, are developed. The
coronal cells and larval muscles are attacked by wandering amoebo-
cytes. The stomach and intestines excrete brown granules into
their respective cavities, and finally lose their cavities and become
solid clumps of degenerating cells. The whole animal is thus reduced
to a thin-walled sac containing, invaginated into it at one point, a
thick-walled sac, which is the former apical disc and is the rudiment
of the future polypide of the mother bud of the colony.

TYPES OF POLYZOAN LARVAE

Before studying the further development of the polypide it will
be well to cast a brief glance at the other types of larvae which have
been described in Polyzoa. All are modifications, one might add
modifications in the direction of degeneracy, of the Cyphonautes type.

Prouho has indeed shown that the species Alcyonidium albidum,
which belongs to quite a different division of Polyzoa (Ctenostomata)
from that to which Membranipora belongs (Cheilostomata), has a larva
which can be distinguished only by minute specific differences from
the larva of Membranipora; and the same is true of the larva of
Hypophorella c.r.pansa, which also belongs to the Ctenostomata but to
a different division from that to which Alcyonidium belongs.

The larva of Flusfrella, a genus allied to Afc>/onidium, is very

XI

TOLYZOA

395

CO

similar to the Cyphonautes. It has a bivalve shell, a well-developed
pyriform organ, and a complete set of muscles ; but the alimentary
canal is somewhat degenerate, the intestine being wanting. The
corona forms a complete ring without cross ridges.

In some species of Alcyonidium, such as Alcyonidium polyoum,
described by Harmer(188'7)

(Fig. 316, A), further de- ap aP9 *

generacy can be seen ; a /

stomodaeum and stomach
alone are present, as in the
larva of Flustrella, but the
bivalve shell is gone, and
the apical organ is a wide,
flat disc. The corona con-
sists of a single ring of
large ciliated cells.

When we pass to Cheilo-
stoniata, like Lepralia,
Bugula, etc., we find that
the gut has entirely
disappeared, and is repre-
sented by a mass of mesen-
chyine cells. The corona
of Lepralia resembles that
of Alcyonidium, but that
of Bugula consists of
enormously tall cells, each
extending through the
whole height of the larva
(Fig. 316, B).

In the Cyclostomata
there is also a gutless
larva, but now the apical
organ is represented by a
deep invagination devoid
of sense cells ; the corona
is represented by a broad
belt of ciliated cells of

Comparatively Small Size ancl the m(''li;in plane of the larva. »;<, apical disc ; fii>.,i,

v . _i : 1 1 _. i j_i_ j_i_ . • _ _ i .1 •

and the pyriform organ is
absent.

Finally in the freshwater Phylactolaemata, where, as in many
other freshwater animals, there is an extremely shortened develop-
ment, we find an oval larva, most of whose surface is covered \vith
fine cilia,, but which has an invagination at the anterior pole whilst
the posterior pole is glandular. The broad ciliated band represents
the corona, the apical invagination the apical organ, which is,
however, entirely devoid of sense-hairs, and from whieh one or two

FIG. 316. — Two degenerate types of larvae of Ecto-
proct Polyzoa. (Combined from figures given by
Korschelt and Heider. )

A, optical section of the larva of Al<-i/<>i,i<Hii in //n/i/imm.
B, optical section of the larva of Iljujiiln jilmiuisu. The dark
streaks represent coronal cells lying between tin- leader

;anglion cells beneath the apical disc; co, corona; i.a,
internal sac ; m, mouth ; j>.n, pyriform organ ; xt, stomach.

396 INVERTEBEATA CHAP.

polypides are already being developed. Fixation takes place by the
posterior glandular pole, and then the walls of the anterior invagina-
tion are suddenly turned back so that the polypide area is exposed.
The retroverted folds adhere to the substratum and force the larva
away from its primary attachment. In this way a huge sucker-like
organ is formed at the posterior pole ; this sucker becomes a
completely closed sac, and then its contents are devoured by
amoebocytes.

It will be seen that in the series of larvae which we have just
described we have to deal with a progressive disappearance of larval
structures, and a progressive hurrying on of adult structures. Thus
in the Phylactolaemata, which constitute the culminating point of the
series, the larval body has become merely a skin enclosing the first
two or three buds. It is obvious, therefore, that in seeking for
light on the past history of the Polyzoan stock we must confine our
attention to the primitive type of larva represented by Cyphouautes.

BUDDING

The metamorphosed Cyphonautes consists of a simple ectodermic
sac with a closed vesicle of columnar cells projecting into it. This
ectodermic vesicle is termed the polypide, and from it the ectodermic
parts of the tentacles, and the whole alimentary canal of the first
person of the colony, are derived. The niesodermal portions of the
tentacles, including the walls of the coelomic canals which they
contain, are derived from a layer of mesoderrn cells (j?o/.mfs, Fig.
315) which clothes the external surface of the polypide. The exact
origin of these mesoderm cells from pre-existing larval mesoderm
has not been determined. The ectodermic sac -like body of the
metamorphosed larva constitutes the zooecium of the first polypide.
The valves of the larval shell are soon shed and are replaced by
the continuous cuticle which constitutes the ectocyst of the zooecium.

The first person of the colony originates therefore as a bud on
the body of the metamorphosed larva ; and, so far as is known, the
development of this bud is quite similar to that of the later buds,
by which the colony increases in size. It follows that in Polyzoa
Ectoprocta, we have not the continuous life-history of an individual
proceeding from the larval to the adult condition, but an alternation
of generations by which a sexually produced form, the larva, gives
rise to an asexually produced form, the first person of the colony.

The manner in which the buds of Polyzoa Ectoprocta develop
has been investigated by many authors. Seeliger (1890), who
investigated the buds of Bugula, has given the clearest account
of the matter, and as his results have been confirmed in almost
every point by the latest observer, Eomer (1906), we shall follow
Seeliger in our account.

When a new bud is about to be formed the new zooecium arises
as an out-pouching of the old one. The cavity of this pouch is

XI

POLYZOA

eventually cut off from that of the parent zooeciuni by a niesoderuiic
septum, but before this happens the first rudiment of the new
polypide appears in the new zooecium as an ectodermic thickening,
which later becomes an ectodermic pouch open to the exterior,
except in so far as it is roofed over by the common cuticle or

•st

FIG. 317. — Stages in the development of the bud of Buyula cmcularia. (After Seeliger. )

A, the early rudiment of the polypide in the form of an ectodermic invagination. B, a later singe :
the rudiment of the polypide is almost shut off from the exterior, and has increased in depth, and its
ini'soderinic covering has become continuous. C, D, two sections through an older polypide in which
the constriction of the rudiment into atrium and gut has begun. C, is through the opening which
remains as the anus. E, section through a still older polypide in which the tentacles have appeared
as ridges in the atrial wall. The section goes through Hie opening which remains as mouth, at,
rudiment of atrium ; pol.mes, mesoderrn ; pol, polypide; oes, oesophagus; ten, tentucles.

ectocyst. This pouch deepens and its mouth closes, and the resulting
sac becomes divided by a constriction into an upper region, which
is the rudiment of the future atrium or tentacle sheath, with its
contained tentacles, and a lower region, which is the rudiment of the
entire gut of the new person.

The sac becomes clothed externally by mesoderm cells; these

398 INVERTEBBATA CHAP.

cells eventually form a coherent layer, but appear to arise as
wandering cells which adhere individually to the external surface
of the polypide. From this mesodermic layer the coelomic canals
of the tentacles and the ring canal which unites them, are derived.
The constriction between gut rudiment and atrial rudiment becomes
so deep at one place as to completely sever the two from each other,
but before and behind this place two openings are left by which
the two rudiments still communicate, and these openings form the
mouth and anus of the new person. The gut rudiment becomes
divided by constrictions into oesophagus, stomach, and intestine.
The atrial rudiment develops the lophophoral tentacles as ridges
projecting into its cavity, and at the completion of development it
reacquires an opening to the exterior. The retractor muscles,
fuuiculus, etc., are derived from scattered mesoderm cells, which
originate from the mesoderm cells of the mother.

Bonier, who investigated the buds of Alcyonidium, differs only
from Seeliger in finding that in Alcyonidium the polypide passes
from the condition of a solid thickening to a closed sac at one step,
and in finding mesoderm cells produced by budding from the
ectoderm as well as from the maternal mesoderm cells. While this
is possible we may conclude that it is unlikely.

POLYZOA ENTOPKOCTA

The group of Polyzoa Eutoprocta comprises only three genera,
viz. Loxosoma, Pedicellina, and Urnatella, and the complete life-history
has only been worked out in the case of Pedicellina. We shall
select as type for special study Pedicellina echinata, the early develop-
ment of which was worked out by Hatschek (1877) whose results
were confirmed and extended by Lebedinsky (1905). The remark-
able metamorphosis undergone by the larva was elucidated by
Harrner (1887).

PEDICELLINA ECHINATA

The egg is fertilized whilst it is still in the ovary, and is pene-
trated by several spermatozoa, but only one unites with the nucleus
while the rest are absorbed. The egg is then dehisced into the
atrium of the parent, where it is retained until it has developed into
a full-grown larva.

The egg segments somewhat unequally, the blastomeres at the
animal pole being much smaller than those at the vegetable pole.
Already when seven blastomeres have been formed a blastula stage
has been reached, the upper half being formed of three small
blastomeres, the lower of four larger ones ; the blastocoele is slit-like.
When, however, segmentation has been completed, there results a
spherical blastula whose lower cells are larger and have larger yolk-
granules than the upper cells. Where the border between these
two kinds of cell is situated, there are to be found two cells distinctly

XI

POLYZOA

399

marked off from both animal and vegetable cells, they are rounded
and have unusually large nuclei which are surrounded by clear areas.
The blastula now slightly elongates so that it is bilaterally
symmetrical, and its vegetative half becomes flattened, and these
two peculiar cells are then situated right and left of the plane of
symmetry. The cells of the vegetative half of the egg become then
iuvaginated, and the gastrula stage is attained. The two large cells
mentioned above are situated at the posterior end of the blasto-
pore, but they now pass into the blastocoele and are the mother
cells of the mesoderm. The blastopore is at first slit -like but

stem

mes

FIG. 318. — Early stages hi the development of the egg of Pedicellina echinatn.

(After Hatschek. )

A, flattened blastula. B, gastrula. C, optical section of later stage nearly sagittal showing the
mother cell of the mesoderm of the right side, the endodermic sac, and the stomodaeal imagination.
I), view of stage in which the blastopore is closing seen from below. E, frontal section of the same
stage ; Up, blastopore ; and, endodermic sac ; rn.es, mother cells of the mesoderm.

gradually becomes restricted in length, becoming closed from behind
forwards. The ectoderm, endoderm, and mesoderm are thus definitely
differentiated from one another.

The ectoderm flattens out except at the aboral pole. Here an
apical plate of cylindrical cells is formed. This was termed the cement-
organ by Hatschek, under a mistaken idea that it was the plate by
which the larva fixed itself. This plate develops cilia but it soon
begins to be invaginated. When the complete larval stage has been
attained the walls of the invagination are still ciliated, but the cells
forming the floor multiply so as to form a mass of small rounded
cells several layers thick ; these are ganglion cells as the develop-
ment of the neuropile around them shows.

400 INVERTEBRATA CHAP.

Shortly after the foundation of the apical plate, the so-called
dorsal organ is formed on the anterior aspect of the aboral pole of
the larva. It develops in exactly the same manner as the apical
plate, that is, as an invaginated plate of cylindrical cells, which, how-
ever, is from the beginning markedly bilaterally symmetrical. The
cavity of the invagination becomes tube-like and its walls are formed
by a single layer of cubical ciliated cells, but its noor becomes con-
verted into a bilobed ganglionic mass which is connected with the
apical plate by two strands of nerve fibrils. This ganglionic mass
may be compared to the brain or cerebral ganglia of Annelida
and Mollusca, whilst the pit, which remains as dorsal organ, may be
compared to the cerebral pit of Molluscan larvae.

Whilst these changes have been going on the blastopore has
become completely closed and the archenteron separated from the
ectoderm ; the ventral ectoderm has become thickened, and it con-
sists in fact of a single layer of cylindrical ciliated epithelium.

On this surface now appear three invaginations, one behind the
other. The front one gives rise to the long stomodaeum or
oesophagus, the cells lining which are all ciliated. The mouth is
surrounded by specially long cilia. The stomodaeum joins the sac-
like archenterou, fuses with it, and opens into it.

The hindermost invagination gives rise to the proctodaeum, the
cells lining which carry short cilia. It is borne on a projecting portion
of the ventral surface known as the anal cone, which, as we shall see,
may be compared to the post-trochal portion of a Trochophore larva.
The archeuteron becomes constricted into a main sac-like portion
which forms the stomach, on the lower wall of which glandular
cells are developed, and a small bud-like intestine which meets and
fuses with the ectoderrual rectum, and so the alimentary canal is
completed.

The central invagination gives rise to the atrium or vestibule,
and is shallower than the others. Its outline is at first round but
later becomes square. Its front wall, which abuts on the hinder
wall of the oesophagus, develops into a ventral prominence known as
the epistome ; and on this is a bilobed thickening, which is connected
round the oesophagus with the dorsal organ by two strands of nerve
fibres, and which will develop into the main nerve ganglion of the
adult.

At the sides of the atrial cavity are a pair of somewhat similar
thickenings, and on its hinder wall, where it touches the rectum, is
a third bilobed thickening. The lateral thickenings are obviously
ganglionic in character, for they become connected with the dorsal
organ, or, as we may now term it, the cerebral ganglion, by nervous
strands. The posterior thickening is the transitory rudiment of
a ganglion which disappears during embryonic life.

The edge of the atriuni carries a row of specially powerful cilia
which subserve locomotion and correspond to the corona of the Ecto-
procta. These cilia are everted when the embryo escapes and becomes

XI

POLYZOA

401

a free swimming larva; liut the ridge of cells bearing them can he
retracted, and then they point inwards towards the atrial cavity.

The mesoderm cells have meanwhile developed into short meso-
dermal bands on each side. According to Lebedinsky (1905) each
of these bauds becomes divided into three spherical somites, and in
each somite a cavity appears, which we may regard as coelornic in
character, just before the larva emerges from the parent vestibule.
The first pair of somites become connected with the atrial cavity by
long ciliated ducts which represent the excretory organs ; the second
pair of somites give rise to the ovaries, and the third to the testes
(Fig. 319). A median vagina is formed by a groove-like gutter in
the floor of the atrial cavity, which
becomes shut off in front but
remains open behind.

Besides the mesoderm that
originates from the mother cells of
the mesoderm, mesenchyme cells, i.e.
wandering cells, are budded into
the blastocoele from the ectoderm at
two points on the posterior aspect of
the aboral surface of the larva.
These cells become transformed into
the larval musculature and corre-
spond to the mesectoderm of
Annelida, Mollusca, and Gephyrea.

Lebedinsky 's statements have
been received with a good deal of
scepticism. It is possible that the
excretory organs do not arise as a
pair of ducts connecting the coelornic tes, testes.
cavities with the exterior, but are

true nephridia ; on the other hand, Hatschek saw and figured the
mesodermal bands arising from the mesoderm mother cells, and it is in
accordance with all that we know of other groups that these bands
should give rise to the genital organs.

We owe the most recent descriptions of the free-swimming larva
to Seeliger (1906) and Czwiklitzer (1909). Both of these authors
are anxious to demonstrate the exact correspondence between this
larva and Cyphonautes. Both point out that the cells forming the
floor of the atrial cavity are glandular, and compare these glandular
cells to the glandular cells of the " sucker " of Cyphonautes. Czwik-
litzer points out further the interesting fact that the dorsal organ is
only at the bottom of a ciliated pit in the retracted condition of the
larva. When the larva is paralysed by adding cocaine to the water
in which it swims and is then preserved, the brain is exposed on the
surface and the ciliated canal is flattened out. Both Seeliger and
Czwiklitzer compare the brain to the pyriform organ of Cyphonautcs.
The justice of this comparison will be considered later. Czwiklitzer

VOL. i 2 u

ex

FIG. 319. — Section of the 'embryo of
Pedicettina echinata, parallel to the
sagittal plane but lying to the right
of it. (After Lebediutsky.)

nt, atrium ; ex, excretory organ ; ex.d,
excretory duct ; uv, ovary ; st, stomach ;

402

INVEETEBKATA

CHAP.

preserved his paralysed larvae in a mixture of the solution of cor-
rosive sublimate and glacial acetic acid, or in Fleming's fluid.

The best account of the metamorphosis of the larva we owe to
Harmer (1887). He found that he could not get the larvae which

st

•muse

CO

comm

rTeph

ac

bog

FIG. 320.— Optical sagittal section of the free-swimming larva of 1'edicdlina echinnta.

(After Czwiklitzer combined from several figures.)

a, anus ; a.c, anal cone ; aji, apical plate ; a},.,/, apical ganglion cells ; at, atrium ; co, corona ;
nm, nervous commissure; d.o, dorsal organ; ep, epistome ; hep, dark granular endoderm cells con-
itmg the so-called liver; int, intestine; m, mouth; muse, muscle fibres; neph, excretory organ;
sb.og, sub-oesophageal ganglion ; s.o.g, cerebral ganglion ; st, stomach.

swarmed out from the vestibules of the parent colonies to fix them-
selves to the walls of the vessels in which he had placed these
colonies; so he resorted to the following device. He procured
colonies of Pcdicellina echinata fixed to the calcareous seaweeds
known as Corallines. He cut off all the superfluous branches of the
coralline and placed the pruned stocks carrying the Pedicellina in

xi POLYZOA 403

vessels filled with sea-water, the mouths of which were covered with
pieces of lineu. The vessels were then placed in tide-pools, and were
left there for one or two days. When at the expiration of this time
they were examined, numerous Pedicellina larvae were found which
had fixed themselves to the Coralline Alga. These were cut out
together with small portions of the substratum to which they
adhered. The Coralline Alga is softened by decalcifying it with acid
alcohol, and then sections can easily be cut through it and the
adhering larva.

The larva fixes itself by the edge of the atrium, which we may term
the mantle, the corona being retracted so that its cilia point inwards.
The mantle edges grow inwards along the surface of fixation so as to
completely close the atrium. The anal cone no longer points down-
wards but, as a consequence of the greater growth of the posterior
surface of the larva, points obliquely backwards. The atrium
becomes divided into a lower portion near the surface of fixation,
and an upper portion with which mouth and anus communicate. After
the complete separation of these two portions the walls of the lower
portion fold inwards, its cavity disappears, and its walls are devoured
by wandering cells. The upper section is then divided into a portion
near the mouth and a portion near the anus ; these two portions are
almost separated by the growth of the epistome and of two lateral
folds which grow out from the sides of the atrial cavity.

As the metamorphosis proceeds the anal division of the vestibule
grows rapidly upwards, and at the same time the retracted apical
plate and brain (dorsal organ) undergo histolysis. The same fate
befalls a good many of the cells lining the larval stomach, they pass
into its lumen and are there reduced to structureless globules. The
apex of the epistome and the tip of the anal cone likewise undergo
histolysis and the cilia borne by the former are lost. When the re-
mainder of the vestibule has rotated so far that it is directed upwards
the adult ciliated tentacles begin to develop as lateral projections on
its sides, and its roof is then broken through by a longitudinal slit ;
and so the atrium, now become the adult vestibule, is once more open
to the exterior. The mouth appears to become closed by the remnant
of the epistome during metamorphosis, but this flap is later perforated.

With open vestibule, developed tentacles, open mouth and anus, the
young Pedicellina has reached the adult stage. Its stalk is formed,
as will be seen if this description has been followed, from the lower
part of the vestibule which has become solid. The formation of fresh
buds takes place from the stalk, and the process is very similar in
essentials to what occurs in the formation of buds in the Ectoprocta.
A protrusion grows out from the stalk into which mesenchyme cells
wander, the whole vestibule and the alimentary canal of the bud
arise from an ectodermal invagination, which becomes covered with
mesenchyme cells which give rise to muscles and niesodermal

organs.

In endeavouring to give a phylogenetic interpretation of the

404

INVEETEBEATA

CHAP.

developmental facts which have been narrated in this chapter it is
obvious that we must commence with the life - history of the

B

so.g

at

at

FIG. 321. — Median sagittal sections through two fixed and metamorphosing larvae of

PediceUina echinata. (After Harmer.)

a.c, iuiiil four; n./i, invaj?inated apical plate; at, atrium ; (if1, oral division of atrium; nft, anal
division (, i atrium; co, corona ; co1, dc^eneratm;;1 fragments of ciliated cells of corona ; (/n, dorsal or.nan,
i.e. fc.rdiral pit; r/i, cpistome ; hep, liver cells; int, iiitc.st.iin1; lr, lateral ridge wliich later, with
epistome, divides the atrium into two halves; m, position of the,. mouth; s.o.g, brain J(supra-
oesophageal'ganglion ; st, stomach ; ten, rudiments of tentacles of the adult.

xi POLYZOA 405

Entoprocta, because only in the case of this group are the larval
organs taken over into the adult.

Now the larva of the Entoprocta, as all investigators admit, is
closely related to the Trochophore type of larva. The apical plate is
identical in both forms, the corona obviously corresponds to the
prototroch, whilst the anal cone of the Entoproct larva may be
compared to the post-trochal region of the Trochophore.

If Lebedinsky is to be trusted (and Hatschek confirms him in
some points) the Entoproct larva in reality corresponds to a post-
trochophoral stage in Annelid development, since the mesodermal
baud already exhibits traces of division into three somites. On the
other hand the evanescent posterior and lateral ganglia, discovered by
Lebedinsky, suggest a comparison with the pleural and visceral
ganglia of Mollusca, and we have already seen reason to imagine that
primitive Mollusca, when they diverged from the Annelidan stock,
may have had incipient segmentation represented by two or three
somites. The " dorsal organ " may be compared to the cerebral
ganglia of the Annelida and Mollusca, which are found a little
distance from the apical plate itself.

But starting from an ancestor still retaining the habit of a Trocho-
phore though possessing a segmented rnesoderm, how are we to inter-
pret the metamorphosis ? The closing of the vestibule or atrium and
the consequent shutting off for a time of both mouth and anus from
the exterior must be a secondary feature, for, during the whole history
of the race, mouth and anus must have been continuously functional.
Therefore, although it is correct to say that in individual ontogeny the
larva fixes itself by the whole of its ventral surface, yet this fixation
must represent, in the history of the race, a prae-oral attachment.

Our Entoprocta, therefore, would be exceedingly primitive
Annelida or exceedingly primitive Mollusca, which had become
attached just in front of the mouth, and which have, like Cirri-
pedia and Crinoidea, undergone such extensive growth of the region
of attachment as to rotate the mouth upwards into a more advan-
tageous position for catching floating prey.

The Ectoproct larva in its primitive form, as exemplified by
Cyphonautes, is also allied to the Trochophore larva ; apical plate
and corona have obviously the same significance as in the Entoproct
larva. But the Cyphonautes represents the Trochophore in an
earlier stage of development than does the Entoproct larva, since it
possesses no true mesoderm derived from pole i cells, and has no
secondary cerebral ganglion.

The attempt to compare the pyriform organ to the dorsal organ
of the Entoprocta, although boldly essayed by Seeliger, must be
pronounced a failure. The pyriform organ, as Kupelwieser has
demonstrated, is not a nerve ganglion at all but a peculiar sense
organ, and its position within the circle of the corona cannot be
compared to that of the dorsal organ of the Entoprocta, which is
outside the circle of the corona.

406 INVEKTEBKATA CHAP, xi

The fixing organ of the Cyphonautes larva is the eversible
sucker, and this is a modification of the ventral surface let'ween
mouth and anus, and corresponding to the region which, in Phoronis,
is everted to form the worm-like body of the adult, and the region
which grows into the long worm-like body of the Sipunculoidea.
This latter group, as we have seen, are certainly, and Phoronis is
probably, derived from a Trochophore stock.

We regard, therefore, the Polyzoa Ectoprocta as a degenerate
group, allied to Phoronis and the Sipunculoidea, which have become
fixed by the ventral surface and have learned how to bud. It
follows that Entoprocta and Ectoprocta, though both derived from
the Trochophore stock, in common with all Annelida and Mollusca,
have acquired a fixed life in different ways and at different periods ;
and are not descended from a common fixed Polyzoan ancestor, but
are two separate offshoots from the Trochophoran stock. It follows
also that Polyzoa Ectoprocta alone can be regarded as having affinities
with Podaxonia, and that Polyzoa Entoprocta cannot be included in
this group, as defined by Lankester (1890).

The fact that in the formation of buds the value of the germinal
layer is quite altered, and that tentacles and atrial wall, along with
the alimentary canal, arise from a common rudiment, will be con-
sidered when the similar phenomena amongst Tunicata (Urochorda)
are discussed.

LITERATURE CONSULTED

Czwiklitzer, R. Die Anatomie der Larve von PediceUina ecMnata. Arb. Zool. Inst.
Wien, vol. 17, 1909.

Harmer, S. F. Sur 1'embryogenie des Bryozoaires Ectoproctes. Arch. Zool. Exp.
series 2, vol. 5, 1887.

Harmer, S. F. The Life-History of Pcdu'ellina. Quart. Journ. Micr. Sci., vol. 27,
1887.

Harmer, S. F. Article, "Polyzoa." Camb. Nat. Hist., vol. 2, 1896.

Hatschek. Einbryonalent\vickliing und Knospung der PediceUina ccliinata. Zeit.
Wiss. Zool., vol. 29, 1877.

Korschelt und Heider. Lehrbuch der Entwicklungsgeschichte der vdrbellosen
Tiere, vol. 2, 1892.

Kupelwieser. Untersuclmngen iiber den feineren Ban und die Metamorphose des
Cyphonautes. Zool., vol. 19, 1905.

Lankester. Zoological Articles (Polyzoa). Reprinted from Ency. Brit. 1890.

Lebedinsky. Die Embryonalentwicklung der PediceUina cchinata. Biol. Centralbl.,
vol. 25, 1905.

Prouho, H. Contribution a 1'histoire des Bryozoaires. Arch. Zool. Exp. series 2,
vol. 10, 1892.

Romer, O. Untersuchungen iiber die Knospung Degeneration und Regeneration
von einigen nieinen ectoprocten Bryozoen. Zeit. Wiss. Zool., vol. 84, 1906.

Schneider. Zur Entwicklungsgeschichte und systematische Stelhmg der Bryozoen.
Arch. Mikr. Anat., vol. 5, 1869.

Seeliger. Bemerkungen zur KnospenentAvieklung der Bryozoen. Zeit. Wiss. Zool.,
vol. 50, 1890.

Seeliger. Uber die Larven und verwaiidtschaftsbeziehiingen der Polyzoen. Zeit.
Wiss. Zool., vol. 84, 1906.

CHAPTER XII
BKACHIOPODA

Classification adopted—
1. Ecardines. 2. Testicardines.

THE group of the Brachiopoda is, by some zoologists, regarded as
being allied to tbe Polyzoa Ectoprocta. Like the Ectoprocta, the
Brachiopoda are fixed by a peduncle or foot which may be regarded
as a ventral protrusion from the body. Like them too they possess
a lophophore, i.e. a lip surrounding the mouth from which arises
ciliated tentacles. They possess a pair of trumpet-shaped execretory
organs which also serve as genital ducts, and are therefore coelomi-
ducts, not true nephridia, and the nerve centres remain throughout
life in connection with the ectoderm.

Brachiopoda might be regarded as au offshoot from the Podaxonia,
and this view is adopted by Lankester (1890). The study of their
development therefore becomes a matter of great interest.

Of only four forms, all belonging to the division Testicardines, is
the complete life-history known ; these are Argiope neapolitana,
Cistella neapolitana, Thecidium mediterraneum and Terebratulina
septentrionalis. The development of the first two has been worked
out by Kowalevsky (1874), but he did not employ modern methods ;
his researches were carried out a long time ago. The development
of Thecidium mediterraneum was described by Lacaze-Duthiers in
1869, and only the external features of the development were noted.
The eggs in all these three species pass through the earlier stages of
their development in brood pouches, and only escape as larvae at an
advanced stage of development. But in the case of Terebratulina
septentrionalis they are shed into the sea, they adhere for a little
time to the chaetae of the mother, and escape as larvae at an early
period in development. Of the development of this species we
possess two accounts, one describing the external features of the
entire development, by Morse (1873), and the other giving the
results of the application of modern methods to the embryonic and
free-swimming larval stages, by Conklin (1902). This form, therefore,
will be selected for special description.

407

408

INVEETEBEATA

CHAP.

TEREBRATULINA SEPTENTRIONALIS

Conklin did not himself collect and preserve the eggs and
embryos ; these were collected for him and preserved in Perenyi's
fluid by Dr. Gardiner. Advantage seems to have been taken of the
spontaneous spawning of males and females when brought into the
laboratory. According to Morse, the egg, when laid, is slightly kidney-
shaped and about ^th millimeter long, and, as seen by Conklin in
the preserved state, is oval.

The segmentation of the egg differs widely from that of any
Trochophore larva so far studied. It is true that it divides into
two slightly unequal blastomeres, then by a furrow at right angles
to this, into four, and then by a circumferential furrow into eight
blastomeres. It is true also that the " cross furrow," characteristic of

B

arch

FIG. 322. — Optical sections of early einliryos of Terebrut ulina septentrionalis.

(After Conklin.)

A, blastula, imagination of the vegetative pole just beginning. B, gastrula, imagination com-
plete : beginning of ridge which divides the archenteron into enteron and coeloin. Arch, archenteron ;
bl, blastocoele ; hip, blastopore ; .?, shelf which delimits enteron from coelom.

spiral cleavage, is sometimes seen in the 4-cell stage. But the type
of cleavage is not constant, and it finally results in the formation of
a blastula in which there are a large number of cells absolutely
indistinguishable from one another, and in which it is impossible to
discriminate an animal from a vegetable pole. Sometimes in the
earlier stages of cleavage four larger cells are observed to be budding
off smaller ones, but the final result is always exactly the same
whatever the mode of cleavage ; in all cases a hollow spherical
blastula is formed which is ciliated all over.

Although no experiments have been made to determine the
point, it seems fairly clear that, in the segmentation of the Brachiopod
egg, the cell divisions do not, as in Annelida and Mollusca, separate
organ-forming substances one from another, but that we have to do
with indeterminate cleavage. We shall become closely acquainted
with this form of cleavage when we study the eggs of Echino-
dermata.

XII

BRACHIOPODA

409

The cells of which the blastula consist are long and cylindrical
and carry long cilia. The cilia are inserted in basal granules of
unusually large size. The blastula becomes converted into a gastrula
by a wide-mouthed invagination. The invaginated cells as they pass
inwards change their form and become cubical, but of course still
retain their cilia. This change of form is the first histological
differentiation observed in development. The archenteron is very
spacious and fills up almost the entire interior of the gastrula, so
that the segmentation cavity or blastocoele is reduced to a narrow
slit. The embryo has now a somewhat conical shape, since, at the
place opposite to the blastopore, it is pointed.

The next change which occurs is the division of the archenteron
into gut and coelom (Fig. 322). This takes place by the outgrowth
of a crescentic shelf of cells one layer thick, arising from what after-

coe

B dm/-
dmgr

ent

FIG. 323. — Later embryos of Terebratuli-na septentriunalis seen from the side —
iu optical section. (After Conklin. )

A, stage in which the enteron is nearly delimited from the coelom, but in which the blastopore is
still open. B, stage in which the blastopore has been closed, leaving a pit in its place, and in which
the hinder part of the archenteron has been obliterated. Up, blastopore; coe, coelom ; d.m.f, dorsal
mantle-fold ; d.m.g, dorsal mantle-groove ; ent, enteron ; 1. coe, left lobe of coelom seen from behind the
euleron.

wards is seen to be the anterior side of the archenteron. This shelf
arises from a position fairly high up on the wall of the archenteron,
and grows backwards and downwards into its cavity. 'It is bilater-
ally symmetrical, i.e. it is equally developed on the right and left
sides. By this outgrowth the archenteron is divided into an oval
gut above, and a broad flat coelom below, which underlies the euteron
and overlaps it at the sides. The two chambers, however, still open
into each other posteriorly, and the lower one communicates with
the exterior through the blastopore.

The next change which occurs is that the embryo becomes
flattened in a dorso- ventral direction, and the coelom becomes
divided into right and left portions in the middle of its course, owing
to the gut being, as it were, pressed through it into contact with
the ventral ectoderm (Fig. 323).

At the same time the blastopore becomes closed, and the manner
in which this takes place is important. It becomes changed in

410 INVERTEBRATA

CHAP.

shape from a large round opening to a narrow slit-like groove. Then
the edges of this groove approach one another and finally cohere in
the posterior part of the embryo. In the anterior portion of the groove
a pore opening into the archenteron persists for some time. Finally
this is closed, but a shallow pit is left, and in this same spot, at a later
date, the invagination to form the stomodaeum arises. In this way
a valuable landmark is created for the correlation of the region of
the larva with reference to the adult organs.

On the opposite side of the larva from that on which the stomo-
daeum is situated — a side which we must regard as the dorsal side-
a depression appears in the form of a transverse groove which is the
beginning of the mantle-groove, and the embryo now takes on the

ent.

sfom

FIG. 324. — Dorsal and ventral views of a larva of Terebmtulina septentrionuUf.

( After Conklin.)

A, dorsal view. B, ventral view, up, apical plate ; coe\ roe?, coeS, the three divisions of the
coelom on the left side; d.m.f, dorsal mantle-fold; d.m.g, dorsal posterior mantle-groove; ent, gilt;
stom, rudiment of the stomodaeum ; v.m.f, ventral mantle-fold ; v.m.g, ventral anterior mantle-groove.

form of a top with a broad anterior and a narrow posterior region.
At the same time the communication between the gut and" the
coelom becomes completely closed.

In the dorsal region the mantle-fold appears as a fold or lip
overhanging the mantle-groove in front. This fold has a crescentic
form, being situated farthest forward in the middle portion, and
inclining downwards and backwards at the two sides. It soon extends
on to the ventral surface in the form of two backwardly directed
folds which meet in the mid-ventral line at an acute angle. The
point where they meet is situated just behind the spot where the last
trace of the blastopore was seen, and where the pit is found which
marks the site of the future stomodaeum (Fig. 324).

When the mantle-fold has been completed, it will be observed
that there is a mantle-groove not only behind it but also in front of it.
The anterior mantle-groove marks off a "head segment," whilst

xii BKACHIOPODA 411

the part of the larva behind the posterior mantle-groove is the " foot
segment," the middle region being known as the "mantle segment."

The posterior groove is deepest on the dorsal side, the anterior groove
on the ventral one (Fig. 325). The mantle-fold grows rapidly back-
wards until it almost completely covers the foot segment. At
four places on the edge of the mantle, two near the mid-dorsal line
and two more laterally situated, invaginations are formed, and the
cells at the bottom of these sacs give rise to long chaetae. These
chaetae were not observed by Conklin, but the sacs were visible in
his sections, the chaetae had dropped out.

Whilst these changes have been taking place the coelom has been
undergoing development. When we last referred to it, it consisted of
right and left sacs which communicated with one another in front
and behind. These communications, however, become closed by the
proliferation of cells into the
cavity of the coelom. The
coelomic cavities become
narrow, almost vestigial, in
the region of the foot, but in
the head region they expand
and take on a trefoil form.
In the mantle region the
coelom sends out dorsal and coe
ventral extensions into the
mantle-folds. This section of

the coelom alone remains wide v™f

j • 1.1. ' P scorn.

and spacious ; the cavities 01

the head and foot coelom Fi«-325.^Lateralviewofalarvaof:rereJraMma

, ... . septentrwnalis. (After Conklm. )

almost disappear in conse-

., , I , . , . ,. Letters as in preceding limnr.

queuce ot the thickening ot

their lateral walls. When viewed from the side, the coelom is seen
to be regularly divided into head-, mantle, and foot lobes, and
there is a specially narrow part in the middle of the foot behind
which it widens out again. This last dilatation is regarded by
Shipley (1883) as forming a fourth segment (Fig. 325).

The gut is a flask-shaped sac, the broad end of which is anterior
and the narrow end posterior. In the latest stage which Conklin
examined, a ventral outgrowth of endoderm cells is formed, extending
towards the pit already referred to, which marks the site of the last
trace of the blastopore. There is no doubt that this is the rudiment
of the endodermal part of the oesophagus.

Just in front of the dorsal apex of the larva the ectoderm is
slightly invaginated. The invaginated cells are very long and slender
and carry a specially long tuft of cilia (Figs. 326 and 327). At
their bases small rounded ganglion cells are cut off, which, how-
ever, remain in close contact with the ectoderm. The plate so formed
is evidently homologous with the apical plate of the Trochophore
larva, and the cells at its base are the rudiment of a supra-

412

INVERTEBEATA

CHAP.

oesophageal ganglion. A quite similar sense -plate is formed in
the mid-ventral line behind the rudiment of the stomodaeum.
Whether this plate bore cilia or not was not determined, but its
cells are the same shape as those of the apical plate, and, from their
bases, ganglion cells are cut off which are the rudiment of the
important sub-oesophageal ganglion of the adult (Fig. 326).

Before this stage has been reached the embryo has become trans-
formed into a free-swimming larva of most characteristic form. The
body is divided by constrictions into three segments. Of these the
anterior, or head segment, is conical and ciliated all over like the hood
of the Actinotrocha larva, but carries in addition an apical tuft of
long cilia ; the second, or mantle segment, carries two long backwardly

erit

cod1

coe~

FICJ. 326. — Frontal and sagittal sections of the larva of Terebratulina septentrionalis.

(After Conkliu.)

Letters as in the two preceding figures. In addition, coe.m, extension of coelom into mantle- fold ;
sb.o.g, rudiment of suboesophageal ganglion.

directed folds, a dorsal and a ventral, both of which are ciliated ; the
dorsal carries the bundles of chaetae on its edge ; the third, or foot
segment, carries no cilia or chaetae. Since the larva possesses no
mouth, and is therefore unable to feed itself, its free life must be of
short duration.

For the account of its metamorphosis we are entirely indebted to
Morse, and, as he did not use the method of sections, we know only
the external features of this period of the development of the larva.
After swimming for some time, not in any case longer than twenty-
four hours, the larva fixes itself to a suitable substratum by the end of
the foot. This " foot " becomes transformed into the peduncle or stalk
of the adult. Tlu-n the mantle-folds lose their ciliated covering, first
on the ventral and then on the dorsal side (Fig. 327) ; then they are
suddenly retroverted so as to project forwards instead of backwards,

xii BEACHIOPODA 413

and so hide, not the foot, but the head segment. On the outer surface
of the mantle-folds the valves of the shell now make their appearance.
The first chaetae are very long ; they are of a provisional nature and
are soon shed, and the sacs containing them disappear, but in their
place there appear more numerous chaeta-sacs with short chaetae,
which persist through life. The head segment becomes less and less
prominent. The first ciliated tentacles of the lophophore make
their appearance at the sides of the head segment (Fig. 328). Others
subsequently appear so as to form a transversely oval ring surrounding
the mouth. A part of this ring extends up on to the base of the
dorsal man tie -lobe, but there is no doubt that the whole of the

vmf

m.a

FIG. 327. — Two larvae of Terebratulina septentrionalis just before arid at the time

of fixation. (After Morse. )

A, free-swimming larva. B, larva at the moment of fixation, ap, apical tuft of cilia ; //, head
segment; ma, mantle segment ; ped, foot segment ; v.m.f, area of the mantle segment which is about
to become the ventral mantle-fold and has lost its cilia.

lophophore must be regarded as belonging to the head segment ;
later the oval ring becomes produced at the corners which constitute
the adult " arms." The pores in the shell, so characteristic of
Brachiopoda, are already to be seen. These are caused by the out-
growth of blind tubes from the mantle coelom through the ectoderm
(coe.c, Fig. 329).

AFFINITIES OF THE BEACHIOPODA

It must be obvious to the reader that there is still a wide and
promising field for further investigation in the elucidation of the
organ ogeny of a Brachiopod. Conklin's investigations, which have
done more to clear up the subject than any other, were done, as we
have seen, on material collected and preserved for him, as an interlude
in his more serious work on Molluscan and Tunicate Embryology.

414

INVEETEBEATA

CHAP.

If some investigator were to devote a summer to the subject and
to repeat Morse's observations on the living larvae, if better methods
of preservation were used and the celloidin - paraffin method of
embedding employed, as described in Chapter II., there is no doubt
that a flood of light would be thrown 011 the subject. Professor Morse
himself, who has deserted zoology for other fields of research, once
expressed to us his regret that no one had so far followed in his
footsteps, and he maintained that the larvae could be reared through
their metamorphosis without any difficulty.

Whilst, however, awaiting the advent of a

zoologist

who will

a.ch

B

v.v:

FIG. 328. — Two young Ti-ri'lu-atn/iii<t m-fiti'iifri<nialis immediately after the metamorphoses.

(After Morse.)

A, specimen showing six bundles of provisional cliaetae. B, specimen showing the origin of the
first tentacles, a.f/i, adult ch;irtm- ; /i, hc;ul segment ; il.i; dorsal valve ; l.ch, larval chaetae ; m, mouth ;
ti-n, lirst tentacles of the lophophore ; c.v, ventral valve ; ped, peduncle.

thoroughly clear up the subject, a few provisional conclusions may
be briefly indicated. Professor Morse himself entertained no doubt
that the Brachiopoda were an ancient offshoot from the Annelidan
stem, basing his conclusion on the presence of distinct segments and
of chaeta-sacs in the larva.

In most Brachiopoda there is no anus at all, although there is a
blind and apparently functionless intestine; but in a few archaic
genera, grouped together as Ecardines, an anus exists. In Lingula
this is situated on one side, near the origin of the peduncle — which
in this genus alone is muscular, — in the groove between dorsal ami
ventral mantle-lobes. In Cr<mia it is situated in the middle line,
at the posterior end of the animal, since in this genus the foot

tei

XII

BRACHIOPODA

415

is absent
of one valve.

segment

and attachment is effected by tbe whole surface

It is obvious, therefore, that the foot segment cannot be regarded

coe.c

ved

v.v.

as a true segment in the Anuelidan sense of the word. It is
probably to be regarded as a ventral protrusion of the body, similar
to the protrusion which forms the greater part of the body in
Podaxonia, with this difference, that in recent Brachiopoda, at any
rate, it remains solid and no part of the alimentary canal passes into it.

But we have already reached the conclusion that the Podaxonia
represent an early offshoot from the
Annelidan stem, and, if the Brachio-
poda are to be regarded as showing
affinities with the Podaxonia, Morse's
general conclusion would be justified
in a roundabout manner.

Conkliu's researches have added
certain points in favour of Morse's
view. The existence of an apical
plate with a tuft of long cilia, and
above all the position of the mouth
as ventral and posterior to the top-
shaped ciliated head segment, which
may be regarded as representing — as
it does in Podaxonia — an enlarged
prototroch, are facts which seem to
point to an essential identity of
structure between the Brachiopod
and Trochophore larvae.

On the other hand,
of the coelom as a division of the
archenteron, and the indeterminate
cleavage, are points in which the
development of the Brachiopod
diverges widely from that of any
Trochophore larva so far studied,
unless Erlanger's results with regard

to the development of Paludina should be finally sustained. They
recall forcibly the development of Echinoderniata.

We shall reserve a final conclusion on the affinities of the
Echinoderniata and Brachiopoda until the development of the former
group has been studied, but we may remark, in the meantime, that
the coelom might be described as a hollow, bilobed but unpaired,
ventral diverticulum of the gut.

If we view it in this light we shall be forcibly reminded of
Erlanger's still unrefuted statement as to the origin of the coelom in
Paludina. We had already arrived at the conclusion that, in the
Trochophore, the origin of the coelomic mesoderm from a single large
mother cell (4d), which was originally situated in the gut wall,

the

origin

FIG. 329. — Young Tcrebratulina septen-
trionalis some little time after
metamorphosis, viewed from the
dorsal surface. (After Morse.)

art, articulating processes of valves — a
notch on each side on dorsal valve ; coe.c,
blind extensions of mantle-coelom perforat-
ing the shell ; d.v, dorsal valve ; ?/!, mouth ;
oes, oesophagus ; ped, stalk ; st, stomach ;
ten, tentacles of lophi.iphurt1 ; ''• (', ventral
valve.

416 INVEKTEBBATA CHAP.

must be interpreted as a reminiscence of pouch-formation, which had
been suppressed because the number of embryonic cells present at
that stage had been diminished.

This consideration brings us to the final point. Determinate
cleavage, in which each cell division separates specific organ-forming
substances, is distinguished from indeterminate cleavage, in which
the individual cell is a subdivision of no importance, by the fact
that in the former type there are fewer and larger blastomeres
present at any given stage than in the latter.

Now the Brachiopod has almost certainly got indeterminate
cleavage of the egg. It would be natural, therefore, to expect that
Bracbiopoda should retain the pouch-method of forming the coeloui.
That the coelom, according to Kowalevsky, is cut off as a pair of
lateral pouches in Argiope, and as a single -bilobed pouch in
Terebratulina, does not seem to be of any particular importance, for
quite similar variations in the method of coelom formation are met
with amongst Echinodermata.

If we imagine that at one time the Ctenophore-like ancestor of
Annelida possessed indeterminate cleavage, and that the change to
determinate cleavage is a later specialization, then we might imagine
that the Brachiopoda were an offshoot from the Proto-annelidan stem
before determinate cleavage had been acquired.

If this conclusion were justified, the Brachiopoda could not be
included amongst the Podaxonia, but would represent an analogous
offshoot occurring at a much earlier date ; and thus Professor
Morse's characterization of the Brachiopoda as "ancient cephalized
worms," contrasted with Gephyrea, Serpulids, etc., as "modern
cephalized worms," would be found to contain a large measure of
truth.

Great light on many obscure questions of Brachiopodan embryology
would be obtained by a successful elucidation of the development of
Ling ula, a genus which has persisted almost unchanged since early
Cambrian times.

The late Professor Brooks (1878), of Johns Hopkins University,
Baltimore, found a free-swimming larva of this form and described
its metamorphosis. This larva, however, represents a much later
stage in development than the free -swimming larvae of other
Brachiopoda, so far studied, because the mantle -lobes are already
retroverted, and the valves of the shell and the first rudiments of the
lophophore are formed. In fact it bears much the same relationship
to the larva of T&rebratulina as the Molluscan veliger larva does to
the Molluscan trochophore. It is to be hoped that some one of the
many brilliant pupils of Professor Brooks may take up their master's
work and carry it to a successful conclusion.

LITERATURE REFERRED TO

Brooks, W. K. The Development of Lingula. Chesapeake Zool. Laboratory,
Scientific Results of Session 1878. Baltimore, 1878.

xii BEACHTOPODA 417

Conklin. The Embryology of a Brachiopod (Terebratulina septentrionalis). Proc.
Amer. Phil. Soc., vol. 4, 1902.

Kowalevsky. On the Development of Brachiopoda. Proc. Imp. Society for in-
vestigating Anthropology and Ethnography, vol. 14. (Abstract by Agassiz), Amer.
Journ. Sci. , 1874.

Lacaze-Duthiers. Histoire de la Thecidie. Ann. Sc. Nat., series 4, vol. 15, 1861.

Lankester, E. R. Zoological Articles, "Polyzoa," reprinted from Encycl. Brit., 1890.

Morse. On the Embryology of Terebratulina. Mem. Boston Soc. of Nat. Hist.,
vol. lo, 1873.

Shipley. On the Structure and Development of Argiope. Mitt. Zool. Stat. Neapel,
vol. 4, 1883.

VOL. I 2 E

CHAPTER X1I1
EOTIFEKA

Classification a d 'opted—

1. Floscularidea. 4. Asplanchnidea.

2. Melicertidea. 5. Scirtopoda.

3. Bdelloida. 6. Ploima.

THE liotifera are a puzzling group of minute animals about whose
affinities most contrary views have been held. The extremely small
size of the adult, and consequently of the egg, has made the investi-
gation of the development extremely difficult, but within compara-
tively recent times Zelinka (1892) has published a most satisfactory
account of the development of Callidina russeola, and this we shall
accordingly select as type. Jennings (1895) traced the cell-lineage
of the egg of Asplanchna Herricki for a few generations, but, as he
did not correlate the regions of the cellular embryo to the organs of
the adult which resulted therefrom, his work is of no value for us.

CALLIDINA IIUSSEOLA

Callidina russeola belongs to the division of Eotifera known as
Bdelloida, in which there is an eversible proboscis in the mid-dorsal
line, and in which the ciliated organ is represented by two semi-
circular retractile hoops placed at the sides of the proboscis, and in
which the body ends in a " foot " terminating in a pair of forceps.
Callidina lays what is, for its size, a comparatively large egg. The
egg-case measures -1 mm. in length, and the whole of the development
takes place after laying ; a period of seventeen days is required
before the completed embryo escapes from the egg-case. Callidina
is an inhabitant of the drops of water which cling to the thickly
matted leaves of moss plants, and the eggs can be found by rinsing
the moss in water and examining the washed-out rubbish under a
low power. It is, however, better to catch adult specimens of
Callidina and keep them in clean watch-glasses until they lay
their eggs.

418

CHAP. XIII

EOTIFEKA

419

These eggs have a somewhat sticky exterior and are apt to
become coated with particles of dust, etc. If the water in which
they lie is kept clean and changed, they will develop perfectly
normally until the perfect Kotifer hatches out. Most of Zelinka's
observations seem to have been made on the living egg. The egg
and its surrounding case are of an oval shape, and at one end there
is a fine circular line in the shell, the plane of which is at right angles
to the long axis of the egg. This marks the spot where the end of

FIG. 330. — Early stages in the segmentation of the egg of Callidina russeola.

(After Zelinka.)

A, 2-cell stage from the side, before rotation. B, 2-cell stage from the side, after rotation. C, D,
3-cell stage and preparation for 4-cell stage, from dorsal surface. E, 4-cell stage, from the dorsal
surface. /'.'», polar body.

the egg-case will come off, as it does, in a lid-like manner, and where
the embryo will emerge.

The development is parthenogenetic : no male has yet been found
in the case of Callidina. Five hours after the egg is laid a single
polar body of comparatively large size is given off from the upper
pole. It does not remain here, however, but rotates, along with the
general contents of the egg, on to a surface which eventually turns
out to be the dorsal surface of the embryo (Fig. 330, B).

Before this has happened the egg-nucleus has retreated from the
spot where the polar body was given off, to the centre of the egg.

420

INVEETEBEATA

CHAP.

Here the first spindle is formed, almost transverse to the long axis of
the egg, and the first cleavage plane is consequently longitudinal and
divides the egg into two cells, a larger, denominated I, and a smaller
one called A, lying side by side. The polar body lies at one end of
this furrow, which, since it is near the pole where the polar body was
given off, we shall call the animal or upper pole of the egg.

With the rotation, however, of the polar body, which has just
been described, the cleavage plane separating the first two blasto-

a

FIG. 331. — Further stages in the segmentation of the egg of Callidina russeola.

(After Zelinka.)

A, 5-cell stage seen from the ventral surface. B, 6-cell stage seen from the right side. C, 9-cell
stage seen from the left side. I), 10-cell stage seen from the ventral surface.

meres also rotates, so that from a position almost parallel to the long
axis of the egg it takes up a position almost transverse to this
axis. In consequence of this rotation the smaller cell A swings round
until it occupies the posterior pole of the egg. Next a small cell is cut
off by a longitudinal cleavage plane from the right side of the larger
cell. This cell is denominated II. It slips down along the right
side to the posterior pole of the egg. Then A divides into two cells,
a and & ; & comes to occupy the posterior pole of the egg, whilst a and
II come to occupy opposite sides of the egg. In this way a character-
istic lozenge-shaped 4-cell stage is formed (Fig. 330).

XIII

ROTIFERA

421

After a pause a smaller cell III is given off from the large cell I
on its ventral side ; this cell then slides back towards the posterior
end and pushes the cell b, which till now has occupied that position,
on to the dorsal surface. Then II divides into lll and II., by an
oblicp:ie cleavage-plane ; but this plane rotates till it is transverse
and IIX is in front of II2. About an hour later a divides into
«x and a.,, and b into ^ and &.,, by planes of division parallel to the
long axis of the egg. Then I gives off, just as it did before, a cell on
the ventral side. This is denominated IV, and it slides back in the
same way as did III to the posterior end of the egg ; b., and bl are
now both dorsal, and a: has rotated till it is in front of «„, and &, is
in front of b, (Fig. 331).

In this 9-cell stage, therefore, the large cell I occupies the
anterior pole of the egg, and behind it are four longitudinal rows of
two cells each, making up the rest of the

I

egg, thus

IV Hj b1.
III II, 6a

The large cell I gives

off still another small cell V on the ventral
side, which passes backwards, pushing III
back so that it occupies the posterior pole
of the egg. Then the three lateral and
dorsal rows of cells, i.e. II: - II.,, al - a2,
and b1 - b.2, divide by cleavage -planes,
transverse to the long axis of the egg, into
rows of four cells each.

Soon III divides into 11^ in front, and
III2 behind, and this raises the ventral row

n

-V,

cells.

IV,

III

The lare cell

-to the number of four
I and the three upper-

most cells of the three dorsal rows, viz.

1'

HP are distinguished

frorn the rest by
of yolk granules

FIG. 332. — Sixteen-cell .stage in
the si'giuentation of the egg
ofCallidina n/t<si-ii/<i. (After
Zelinka.)

Where a cell has divided into
right and left sisters these are
marked with the .suffixes >• and /.

the greater abundance
in them.

The next change is the doubling of the ventral row by cleavage-
planes parallel to the long axis of the egg. We have now five
longitudinal rows of four ceils each, two of these being ventral and
three dorsal.

But soon the dorsal rows begin to be doubled in the very same
manner ; the granular cells, however, usually remain undivided, but
occasionally become divided into right and left sisters as shown in
Fig. 333, while the cell I gives off, for the last time, a cell VI on the
ventral side ; the latter slides back in the usual manner and presses
the daughters of III1 and III., on to the dorsal surface. The effect
of this is to shove forward the capping cells of the dorsal rows, which,
as we have already seen, are distinguished from the rows to which they
belong by being more granular. Thus, pushed forward, this crown of
three granular cells begins to overarch the front end of the large cell I.

422

INVERTEBEATA

CHAP.

The blastula stage may now be said to be attained. It consists
of the large cell I, of six dorsal rows of three cells each, capped by
three granular cells, of two ventral rows of four cells, and of an odd
cell VI in the mid- ventral line.

Gastrulation now begins by the retiring of the cell I from the
surface. This cell may now be denominated E, as it is the mother
cell of the endoderm. This cell may, however, before its inward
movement begins, be divided into front and posterior cells. Whether
this has occurred or not it speedily does divide in this way, and then
by longitudinal planes into right and left halves, and then by further
transverse planes, till a mass of eight cells has been produced.
Then the three granular cells, if they have not divided before, now

FIG. 333. — Two views of embryos of Callidina russcola showing the process of gastrulation.

(After Zelinka.)

A, dorsal view of an embryo in which Die endoderm cell (I = E) is just sinking inwards. In this
embryo the granular cells cij, l}lt and ll! have each divided into right and left sister cells. This is ex-
ceptional. Tliis division usually does not occur until somewhat later. B, ventral view of a somewhat
later stage in the process of gastrulation. The granular cells have passed round the anterior end of
the embryo on to the ventral surface. The endoderm cell has divided into anterior (E!) and posterior
halves (Eg), and is almost completely enclosed by ectoderm, ijr, granular cells ; p.b, polar body.

divide each into two cells lying side by side, and the two larger rows
of ventral cells are also subdivided by longitudinal planes giving rise
to four rows. The six granular cells become compressed into a mass
and are no longer arranged in a crescent form (Fig. 333).

This mass is the rudiment of what we may term the primary
stomodaeum. It becomes forced from its anterior position on to
the ventral surface by the backward pressure of the cells on the
ventral surface — for these ventral cells continue their initial tendency
to push backwards and to pass on to the dorsal surface at the posterior
pole of the egg ; thus they force forward the rows of dorsal cells, and
it is this pressure which forces the anterior granular cells downwards
round the front end. To reach this stage requires twenty-four hours
from the time that the egg is laid.

XIII

EOTIFERA

423

The next change which occurs is the invagination of the
rudiment of the primary stomodaeum. The layer of clear ectoderm
cells now forms a complete mantle all round the egg. The granular
cells divide and form a two-layered plate of cells lying obliquely
across the egg. Soon afterwards the outer clear ectoderm, at the
spot where the granular cells were covered over, is invagiuated in the
form of a wide funnel, which is the secondary stomodaeum (Fig. 334).

Soon afterwards the whole ventral surface becomes concave, and
in this way the rudiment of the tail, which occupies the hindermost
part of the concavity, is marked off from the rest of the body.
The front border of the concavity, which is at the same time the

stom?

and

FIG. 334. — Optical sagittal sections of two embryos of Cull id I uu ru.iscnla after the process
of gastrulation has been completed. (Alter Zelinka.)

A, earlier stage. B, later stage: the secondary stomodaeum is formed and the ditterenti.-itioti
between head and tail has begun, luud, rudiment of the tail; end, endodernuil cells; ijr, granular
cells ; 7/i., mouth ; stnni1, primary stomodaeum consisting of the granular cells ; xtum", secondary stomo-
daeinn consisting of ordinary ectoderm.

hinder border of the mouth, is the rudiment of the under lip. The
tail, once begun, grows rapidly forwards, so that the embryo is bent
double (Fig. 334).

In front of the mouth an overhanging lobe of cells becomes
prominent ; this is the rudiment of the apical plate out of which
both proboscis and trochal plate grow. It is kidney-shaped in
outline, its longest axis being transverse to that of the embryo, and its
concave border being in front. The concavity deepens until the plate
is obviously bilobed (Fig. 335).

Meanwhile the endoderm cells have been undergoing division, and
they become grouped into two masses, the front one being derived
from the anterior four cells and the hinder from the posterior four.
The posterior mass of cells is contained in the tail or foot, whilst on

424

INVEKTEBEATA

CHAP.

caud

the anterior mass rest, directly, the mass of granular cells forming the
still solid rudiment of the primary stomodaeum. From the sides of
the anterior mass two solid outgrowths are developed, which are the
rudiments of the genital organs, i.e. of vitellarium and germarium ;
for in Kotifers, as in Platyhelininthes, a portion of the genital rudiment
consists of rudimentary ova, which serve as food to the few ova
capable of development, and is termed the vitellarium.

The ectoderm cells in the dorsal region, just behind the " apical
plate," multiply rapidly and project inwards as a solid invagination.
This is the first rudiment of the brain. One day later a second,
larger invagination of the ectoderm takes place in the centre of
the apical plate. It is nearly solid, but a slight hollow appears

at the surface which soon flattens
out. This second ectodermal in-
vagination is the second rudiment
of the brain ; it impinges on the
first, which covers it as a kind of

she»th (Fif- 336>

Soon alter, the inner stomodaeal

rudiment assumes the form of an
oval body, in the centre of which a
fine slit-like cavity appears, which
is in direct communication with the
secondary stomodaeum and mouth.
The primary stomodaeum is now seen
to be the rudiment of the peculiar
pharynx termed the mastax, char-
acteristic of the Kotifers. Some
portions, however, of this stomodaeal
rudiment remain over after the
formation of the pharynx, and at a
later stage give rise to the salivary
glands. The cavity in the pharynx
grows wide, and it is curved in such a way as to leave a large median
hump on its floor. The hump becomes covered with a thick cuticle,
and this cuticle is the first indication of the trophi or jaws.

The head region now begins to grow rapidly. Indeed, the develop-
ment might be said to be characterized by an alternate growth of
the head and foot. The growth takes place in the middle of the
apical plate and forms an elevation which is the rudiment of the
proboscis. The remainder of the apical plate flattens out and forms
a shelf around this elevation. On this shelf at a later period the
trochal cilia are developed, and the place where they will arise is now
indicated by two semicircular strips of cuticle. This shelf is therefore
the rudiment of the trochal disc (Fig. 337, A).

The cells forming the front eudodermal rudiment lose their outlines
and form a syncytiurn ; they then develop a cavity in their interior
which is the cavity of the mid-gut. About the same time, on the

FIG. 335. — Ventral view of embryo of
Callidina russeola somewhat older
than those represented in Fig. 334.
(After Zelinka. )

up, rudiment of apical plate ; mud, rudiment
of tail ; m, mouth.

XIII

EOTIFERA

425

dorsal side of the foot, a hollow invagination of ectoderm appears,
this is the proctodaeum, that is the rudiment of the anus and
hind-gut.

We have already seen that the hinder endodermal rudiment is
contained in the foot, but before the anus is formed it begins to lie
displaced by a solid terminal invagination of ectoderm, which is the
rudiment of the foot gland.

In the following period of development the head region under-
goes complicated developments. The proboscis is bent ventrally.
Between it and the cuticular strips, mentioned above, a solid invagina-

ten.

cer*

tr-

cer1

end*

FIG. 336. — Optical sagittal sections through two late embryos of Callidina russeola in
order to show the formation of organs. (After Zelinka. )

A, stage of predominant growth of the tail. B, later stage : predominant growth of the head
region, rniul.ijl, foot gland ; cer1, cer2, first and second rudiments of the cerebral ganglion ; end1, endo-
dermic rudiment of the gut ; end'2, endodermic rudiment of the excretory bladder ; yon, genital rudi-
ment; jiroli, rudiment of proboscis : provt, proctodaeum; sal, salivary gland ; .•-/"/«', inner stomodaeum
or mastax ; .s/nm-, outer stomodaeum ; ten, tentacle ; //•, border of region of apical plate which gives
rise to the "wheels"; trojih, rudiment of one of the trophi or .jaws.

tion of ectoderm appears on each side of the trochal disc. Then the
whole head region is retracted and surrounded by an upgrowth of
the ventral lip, which, however, does not quite reach the dorsal side.
Later this upgrowth develops the outer cilia known as the
cingnlum. Still later, however, the whole head region — proboscis,
and apical shelf, is again protruded ; and the cuticular strips are
specially thickened at each side, where the shelf shows an indentation.
The ectodermal thickenings between these and the proboscis are
protruded as hemispherical bosses. Subsequently these are again
invaginated, and remain so till the embryo is born, when they are
finally protruded. They are then surrounded with cilia, developed

426

INVERTEBRATA

CHAP.

from the regions of the cuticular bands, and form the " wheel-organs "
of the adult (-Fig. 337, B). They eventually become connected with
each other by a very narrow upper lip, which runs above the mouth
and beneath the proboscis in such a manner that the latter is excluded
from the trochal field. The dorsal feeler, or antenna, is formed at
the spot where the first rudiment of the brain still retains a
connection with the ectoderm.

The muscles all appear to be of ectodermal origin. Those first
observed by Zelinka were longitudinal fibres running from the
" wheel-organs " to the middle of the body. Circular muscles are

caud

stom

end

FIG. 337. — Ventral views of two embryos of Callidina russeola at a stage not long
before hatching. (After Zelinka.)

A, younger stage: stage nf invagination of rudiments of wheel-organs. B, older stage : slage of
evagiiiaticm of rudiments of the wheel-organs and of preponderant growth of the tail, if, anus ; nvuil,
tail; I'ltixLf, caudal fork; end1, endodennal stomach; /'/'<>'<, rudiment of proboscis ; stum, secondary
stomodaeum ; tr, cutifular band marking place where cilia of the "wheels" will appear later.

developed later from ectoderm cells, at regular intervals ; these cells
retain their plasma and their individuality, in contradistinction to
most of the other ectoderm cells which flow together and form a
thin syncytiuin, the so-called " hypodermis."

The first traces of the excretory organs appear comparatively
later as two streaks of dull glistening cells, situated at the sides of the
pharynx. Subsecpaently they are developed into the coiled canal
and adherent soleuocytes, of which in the adult there are eight on
each side. The bladder into which they open is derived from the
endoderni contained in the foot region ; this endoderm has been pushed
forward by the development of those ectoderm cells which constitute
the foot gland.

xni ROTIFERA 427

AFFINITIES OF THE ROTIFERA

Zelinka endeavours to show that the course of development which
he describes proves, that Callidina, and therefore presumably all other
Rotifera, show affinities to the Trochophore larva of Annelida and
Mollusca ; that, in a sense, they are what Huxley termed persistent
Trochophore larvae. That there is a general resemblance between
certain Rotifers such as Callidina when adult, and Trochophore
larvae cannot be denied ; but if this resemblance be an indication of
real affinity, then we must regard the early development of Rotifera
as profoundly modified ; for there is no resemblance between the
early development of this group and the early development of a
typical Trochophore larva, with its specialized cleavage, characterized
by the formation of four macronieres and three quartettes of ecto-
derrnic micromeres given off from near the animal pole of the egg.
The small cells in the Rotiferan egg are given off, one by one, from
the -vegetative pole, and rotate round the posterior end of the egg on
to the dorsal surface. The excretory organs of the Rotifera look like
the archnephridia of the Trochophore larva, but their origin from the
ectoderm has yet to be demonstrated. Unlike all other nephridia
they do not open to the exterior, but discharge into an endodermic
sac — the bladder, which we may compare to a coelomic sac, which
still retains its opening into the gut. The early differentiation of the
rudiments of the genital organs is a common feature in animals
without larval development and with a very short life-cycle. On the
whole, we may conclude that much more work remains to be done on
the development of types of Rotifera with different forms of trochal
disc, before the hypothesis of the affinity of the group with Trocho-
phore larvae can be regarded as substantiated.

LITERATURE REFERRED TO

Jennings. The Early Development of As^lanchna Herricki. Bull. Mus. Coinp.
Zool. Harvard, 1895.

Zelinka. Studien Uber Radertiere III. Zeitschr. fur wiss. Zool. vol. 53, 1892.

CHAPTER XIV
CHAETOGNATHA

THE little group of the Chaetognatha, or " Arrow-worms," cousistiug
of Sagitta, Spadella, and Jfrohnia, is one of the most isolated in the
animal kingdom, and its affinities are extremely difficult to determine.
All we can say with certainty is that its members exhibit a very
primitive type of adult structure and a still more primitive develop-
ment.

SAGITTA

The Chaetognatha are with few exceptions pelagic animals and
are of world -wide distribution. The development of the genus
Sagitta has been worked at by Kowalevsky (1871), Btitschli (1873),
and by Hertwig (1880), who described what could be made out from
observations on the living embryos and from preserved specimens
mounted whole. The subject has been taken up again by Doncaster
(1902), who used the method of sections and who has given us a fairly
complete account of the development of Sagitta, lipunctata. It must
be admitted, however, that some of Doncaster's figures are far from
satisfactory, and it is greatly to be desired that a revision of the
subject should be made.

Doncaster's method of procuring the eggs and embryos was,
to secure a number of adults and keep them in a jar of clean sea-
water, in which they lived very well for a day or two, and then to
siphon off the bottom layer of the water and to look for the eggs in it.
Doncaster preserved the eggs and larvae in a concentrated solution
of corrosive sublimate to which 5 per cent of acetic acid was added.
He used the method of double embedding in celloidin and paraffin,
so frequently recommended in this volume and described in Chapter II.

Practically the whole development of Sagitta is completed within
the egg:membrane, and when the embryo emerges and becomes a
larva it differs from the adult chiefly in size and in the absence of
developed genital organs. The whole development up to hatching-
only occupies about two days.

The egg, which is '2 mm. in diameter, segments perfectly regularly
into blastomeres of approximately equal size. A blastocoele

428

CHAP. XIV

CHAETOGNATHA

429

appears at the 8-cell stage, and the result of segmentation is the
production of a spherical hollow blastula which, it may be remarked
incidentally, is not unlike the blastula of Ampliioxii.s, although at
once distinguishable from it by its greater size. One side of this
blastula flattens and on the flat side an invagination takes place, and
the blastula is thus converted into a gastrula.

The invagination, which is the rudiment of the archenteron,
increases in depth till it practically fills up the entire blastocoele and
the eudoderni is pressed close against the ectoderm. The whole gastrula
then elongates, the blastopore narrows, and the embryo assumes a
fusiform shape, being more or less pointed at the anterior and
posterior ends and broadest in the middle.

At the same time the mother cells of the genital organs make

enl

coe

Flu. 338. — Optical sections of early embryos of Sogitta bipunctata. (After Doncaster.)

A, gastrula showing the two mother cells of the genital organs. B, embryo in which the arclienteron
is being divided by lateral folds into coelomic sacs at the sides and enteron in the middle, lilji, blasto-
pore ; coc, coelomic sac ; ent, enteron ; .'/, mother cell of the genital organs.

their appearance as a pair of large cells which project into the cavity
of the archenteron ; they occur in a position about one-fourth the
length of the embryo From the anterior end. They are extruded from
the wall of the archenteron and are therefore endodermal in origin
(Fig. 338). They touch each other and are, of course, situated sym-
metrically with regard to the median sagittal plane of the embryo,
but, according to Doncaster, they are nearer either the dorsal or the
ventral surface of the embryo ; he could not decide which, for he was
unable to find any definite landmark to discriminate between dorsal
and ventral surfaces. The very early appearance, as peculiar cells,
of the rudiments of the genital organs in many groups, such as those
treated in this and in the preceding and following chapters, has led
to interesting speculations as to whether a reproductive substance is
not separated from a somatic substance at the very beginning of
development. This problem has been attacked, in the case of the
development of Sagitta, by several authors, of whom Buchuer has

430

INVERTEBKATA

CHAP.

given the most recent and satisfactory account (J910). According
to him, during the ripening of the egg, one of the primitive germ
cells becomes embedded in its cytoplasm and degenerates, leaving, as
remains, a deeply staining oval body (nut, Fig. 339). When the
egg undergoes segmentation this body is found in one of the first
two blastomeres. In subsequent divisions it is not divided, but
always passes into one blastomere. When, however, the blastula
stage is passed and gastrulation has been accomplished, it is divided
between two cells, and these cells are the mother cells of the genital
organs. It thus appears that in Sagitta, as in the Crustacean Poly-
phc'inns (see p. 193), the cell destined to produce the genital organs
is distinguished, not by peculiarities of its nuclear substance, but
by the possession of an extra store of nourishment.

The next change which
occurs in the development is
the formation of the coelom.
This takes place by the de-
velopment of a pair of inwardly
directed folds in the archen-
teric wall, which start from its
anterior border, one on each
side of the middle line, and
grow backwards as a double
wall. In this way the archen-
teron becomes divided into a
median chamber, the digestive
tract or gut, and two lateral
chambers, one on each side,
the coelomic sacs. At first
all three chambers open into
a common undivided chamber
behind.

At the same time the
shape of the embryo changes,
because as these folds develop
they use up a considerable
portion of the front part of the archenteric wall, which had projected
forward in a conical process. As a consequence, the anterior pointed
end of the embryo becomes changed into a broad, very slightly
convex surface, whilst the posterior end remains pointed.

The mother cells of the genital organs are in contact with the arch-
enteric wall almost at the point where the folds originate, and as these
grow backward they carry the mother cells of the genital organs before
them, so that these primitive germ cells are carried back into the
hinder half of the embryo. There they pass into the coelomic division
of the archenteron on each side, round the bend of the fold, and each
then divides into an anterior and a posterior half (gv gz, Fig. 340).
Whilst this has been occurring the whole embryo grows consider-

9

FIG. 339. — Cross section of the blastula of
Sagitta bipunctata (?) in the 16-cell stage,
showing the determination of the mother cell
of the genital organs. (After Buchner. )

g, mother cell of the genital organs ; nut, remains
of nutritive cell embedded in the mother cell of the
jrenital organs.

XIV

CHAETOGNATHA

433

ably iti length, so that the anterior convex end bears but a small pro-
portion to the total length. The central division of the archenteron
becomes closed off from the two lateral divisions behind, by the
approximation and union of the inner walls of its folds, and in this
way the gut is separated from the coelomic sacs.

The front portions of the coelomic sacs, lying at the sides of the
stomodaeurn, become separated from the rest and form a pair of round
thick-walled head-cavities. The cavities are soon obliterated, but
their walls give rise to the muscles which move the curved setae
situated near the mouth, which give the name to the phylum.

The masses of mesoderm which represent the head -cavities

stem.

coe

Fin. 340. — Optical section of older embryo of Sagitta bipnnctufn, showing the formation of
the "head -cavities" and of the stomodaeum. (After Doncaster.)

coe, coelomic sac ; ent, enteron ; j/i, mother cell of ovary ; g2, mother cell of the testis ; h.r, hruil-

cavity ; stom, stomodaeum.

touch each other dorsally, but ventral ly are separated by the
stomodaeum1, so that they resemble a horse shoe in shape. Traced
backwards these masses of head-mesoderm are seen to overlap the
front ends of the hinder portions of the coelomic sacs which are nearer
the middle line.

The blastopore closes completely ; its last trace is on the ventral
surface, far back but not quite at the posterior end, and at the same
time an ectodermic invagination makes its appearance at the anterior
end of the embryo ; this is the stomodaeum, which grows backwards
and breaks through into the gut.

The coelomic sacs continue for a short time to open into a common
sac behind, which occupies about one-third the length of the whole
embryo, but soon this single sac becomes divided into right and left
halves by the backward growth of a septum. This septum is formed

432

INVERTEBRATA

CHAP.

s.o.g

-muse

7

vac

sens

by the coalescence of the right and left
archenteric folds, and it might almost be
regarded as a solid portion of the gut.

The adult Sagitta, exhibits a differen-
tiation of the body into head, trunk, and
tail. The head swelling is initiated in
the embryo by a great anterior dorsal
ectodermic proliferation, which later
gives rise to the brain or supra-
oesophageal ganglion (s.o.g, Fig. 341).
It is increased by the formation of a
lateral swelling on each side, forming
a ridge. These two ridges later unite
to form the cephalic hood. Finally,
owing to the fact that, as the embryo
increases in length, the stomodaeum
retains its cavity whilst the rest of the
gut becomes compressed to form a
vertical solid band, and the cavities of
the coelomic sacs also temporarily dis-
appear, the breadth of the head region
as contrasted with that of the trunk
is emphasized, and the head swelling
stands out distinctly. This suppression
of the cavities seems to be largely due
to the circumstance that, whilst the
embryo is growing in length and
becoming curved, it is still confined
within the egg-shell.

The ventral ganglion makes its
appearance as a thickening of the
ectoderm, stretching from immediately
behind the head to nearly the region
where the anus is formed, and taking up
two- thirds of the length of the embryo
(v.g, Fig. 341). The ectoderm cells become

FIG. 341. — Ventral view. Larva of Sayitta enflata
on the fourth day after hatching, in order to
show the origin of the nervous system and the
separation of the trunk coelom from the tail
coelom. (After Doncaster. )

a, position of the anus ; l>.i; body coelom ; ent, alimentary
canal ; /i, /2, anterior and posterior fins; jri, mother cell
nf ovary; ;/-, mother cell of tin- test.es ; ///,-, masticatory
hooks ; -iii; month ; mnsr, masticatory muscles developed
from the head-cavities ; sens, sense-organ (tactile ?) ; sep,
transverse septum dividing body coelom from tail coelom ;
s.o.g, supra-oesophngeal ganglion ; t.c, trunk coelom ; rm;
vacuolated cells (floating tissue) ; e.g, ventral ganglion.

xiv CHAETOGNATHA 433

columnar in this region and their nuclei retreat to their bases, where
they undergo rapid division and give rise to small rounded ganglion
cells. This proliferation does not take place evenly all over the
ventral surface but along two parallel lines, and we are involuntarily
reminded of the double nature of the Annelid ventral nerve cord.
Sparsely scattered over the body are groups of sensory hairs, arranged
like fans, transversely to the long axis of the body. These are more
numerous on the head. At their bases groups of sensory nuclei can
be seen.

At this stage the young tiagittct is hatched. If the foregoing
description has been followed, it will be seen that it is a solid worm
very unlike the adult, and therefore merits the name of larva. It is
about 1 mm. long, and it swims near the surface of the water,
propelling itself by lateral jerks of the tail fin, which is already
developed. At the bases of the mesoderin cells in the trunk and tail
the fine refractive muscular fibrils can already be made out. They
all run longitudinally.

After swimming for about two days the larva undergoes a com-
paratively rapid change which makes it much more nearly like the
adult in structure. Cavities suddenly reappear both in the
mesoderin of the trunk and in that of the head, and so the larva
becomes inflated and more transparent.

The cephalic hood becomes a prominent fold, and under it a
pair of hooks is to be seen on each side. These hooks gradually
increase in number by the addition of new ones in front, till the full
number characteristic of the species is attained. At each side of the
mouth a rounded ectodermic thickening appears, which is the so-called
lateral ganglion. The eyes also appear as minute black specks. The
cavities in the head disappear again, and the head niesodermal cells
become arranged in definite bundles, forming muscles for moving the
hooks.

As the larva grows in length the ventral ganglion becomes
relatively shorter and the ectoderm cells in front and behind it
become vacuolated so as to form a kind of floating tissue (vac, Fig.
341). Such vacuolated cells are found all over the trunk through-
out life in Spadella draco, but of course they disappear later in life
in Sagitta.

In the tail region the tail fin becomes large and prominent and
extends a good distance forward. It is separated by a gap from two
lateral fins which have appeared, one on each side. In the gap on
each side is situated a large tactile organ, borne on an ectodermal
prominence (sens, Fig. 341).

On the fourth day the genital cells, which up till now have been
disposed in two pairs, an anterior and a posterior pair on each side, begin
to migrate across the body-cavity from its splanchnic to its somatic wall.
As this takes place a lateral septum is formed, cutting the coelom on
each side into trunk and tail portions, and separating the anterior
genital cells on each side, which are the rudiments of the ovaries,
VOL. I 2 F

434 INVERTEBRATA CHAP.

from the posterior ones, which are the rudiments of the testes. This
septum is probably formed as an outwardly projecting fold of the
splanchnic mesoderrn, possibly it may be a modification of portions of
the thin envelopes of the genital cells, which envelopes are themselves
thin layers of cells derived from the splanchnic layer of the mesoderni.

According to Doncaster, the hood which surrounds the head is
formed by a splitting off of an outer layer of cells from the ectoderniic
thickening on each side, and the head coelom persists for a considerable
time and it is its outer wall which is metamorphosed into the
masticatory muscles.

The alimentary canal reacquires its cavity about the eighth day,
and on this day its posterior end bends ventrally and comes into
contact with the ectoderm, where the anus is formed. On the head
at the same time there appears a double curved line of closely packed
nuclei, in the form of a horse-shoe open backwards, and this constitutes
the olfactory organ.

Doncaster was unable to keep the young Sagitta alive for a
longer period than fifteen days, and up till this period no further
changes had taken place in the genital rudiments. The further
development of these organs was determined by fishing young
individuals from the Plankton.

By a comparison of these with the latest stages reared from the
egg it is seen that each of the four primary genital cells divides so as
to form a little mass of cells. The masses of cells representing the
ovaries grow forwards, those representing the testes grow backwards.
Incomplete longitudinal septa appear in the tail coelom on each side,
and bunches of cells drop off from the testes and float in the tail
coelomic cavity, where they undergo all the changes which lead to
their transformation into mature spermatozoa.

The vasa deferentia appear as ectoderniic thickenings in the space
between the lateral fin and the tail fin on each side. This thickening
splits into two layers with a cavity between them. In front this
cavity is exceedingly narrow, and here it eventually acquires an
opening into the coelom. Behind it acquires an opening to the
exterior, and this opening is formed at a spot in the course of a
longitudinal groove which appears on its outer wall.

The ovary becomes differentiated into two well-defined layers,
an inner and outer, between which is a loose ill-defined mass of cells.
The outer layer resembles an epithelium and consists of small cubical
cells abutting against the outer wall of the trunk coelom. The inner
layer consists of tall columnar cells which are the mother cells of
the ova.

As the ova enlarge and mature they become pressed out of this layer
of epithelium, and are found projecting from the surface of the ovary
to wards the body-cavity, though covered with a structureless membrane.
The loose cells which intervene, especially at the base of the ovary
between the germinal epithelium and the ectoderm, eventually develop
a cavity and form the oviduct. This grows backwards and at

xiv CHAETOGNATHA 435

maturity reaches and fuses with the ectoderm at a point where the
female opening is formed. Buchner (1910) has found that the large
ova pass into the naprow oviduct through narrow, slit -like openings
which are only visible at the moment of passage. From the descrip-
tion just given it follows that the male ducts are of ectoderrnal
origin, but that the origin of the female ducts is doubtful, for the
precise origin of the loose cells which give rise to them has not been
ascertained.

AFFINITIES OF THE CHAETOGNATHA

As mentioned in the beginning, the affinities of the Chaetognatha
are very obscure. The early development so far, the segmentation
of the egg, the formation of the archenteron by imagination, and the
formation of the coeloni as lobes of the archenteron, is of a very
primitive type and has been compared to that of Brachiopoda and
Echinodermata. What justice there may be in the latter com-
parison will be considered when the development of Echinodermata
is described.

With regard to Brachiopoda, Conklin lays stress on the difference
between a single anterior septum dividing gut from coelom in
Brachiopoda and the two lateral folds in Chaetognatha, but this
difference is annulled if, as Kowalevsky describes, the coelom in the
Brachiopod Aryiope is separated from the gut by two lateral septa.
But the posterior position of the last traces of the blastopore, and
the early appearance of the stomodaeum, are two great differences in
development which separate Chaetognatha from Brachiopoda.

Another great difference is the total absence of cilia in the
embryo of Sayitta. This is probably partly correlated with the fact
that the development of Sagitta, in spite of its primitive features,
must be extremely shortened, for the larva, though it differs from the
adult in its fuiictionless alimentary canal and solid mesoderm,
nevertheless has the same mode of life as the adult. On the other
hand, in Brachiopoda, as indeed in nearly all the groups of the
animal kingdom which we have as yet studied, the larva has quite a
different mode of life and different locomotor organs from the adult.
The very early differentiation of the genital cells is another sign of
shortened development.

Hertwig compared the Chaetognatha to an Annelid with three
segments, and a comparison has also been suggested between the three
pairs of body-cavities in Chaetognatha and the three segments of the
Brachiopod larva. But with whatever justice such a comparison can
be applied to the head and trunk segments, it is doubtful, as Doucaster
wisely remarks, how far this explanation can be applied to the
separation of trunk and tail segments ; for this latter separation occurs
in Chaetognatha long after the separation of the head-cavities, and it
appears to be a device to separate male and female reproductive organs.

Giinther (1907) has written a long paper to try to prove that
Sagitta is related to the stern of the Mollusca. As the parent stems

436 INVEETEBEATA CHAP, xiv

of Mollusca and of Annelida are identical, this conclusion is not so
different from that of Hertwig as might at first sight appear to be the
case. But Giinther's conclusions are based entirely on interpretations
of adult anatomy and ignore the question of development, in which
Sagitta differs absolutely from any Mollusc so far studied. The facts
that Sagitta is essentially a chitinous animal which nowhere develops
cilia, and that its locornotor organs are both developments of this
cuticle, constitute a deep gulf between it and any of the soft-
skinned Mollusca.

It has been suggested that the Neinatoda have affinities with the
Chaetognatha. The arguments for and against this will be considered
in the next chapter, when the development of Nematoda will be
described. But even if we should finally decide that such an affinity
exists, it would throw no light on the origin of Chaetoguatha, because
in that case the Nematoda would have to be regarded as much
modified and degenerate Chaetognatha which had taken to burrowing
and parasitic habits.

The conclusion to which we are led, the arguments for which will
be developed later, is, that in immensely renXote times there existed
a stock of free-swimming animals in which the coeloui still was in
open communication with the gut. This hypothetical stock may be
called the Protocoelomata, and from it all the groups of coelomate
animals would be descended. If this be correct, the Chaetognatha
would represent a small, comparatively unmodified offshoot from
that stock, a group which has been able to hold its own until the
present day.

LITERATURE REFERRED TO

Buchner, P. Die Schicksale des Keimplasmas tier Sagitten in Reifmig, Befniclitung,
Keimbahn, Ovogenese und Sperniatogenese. Festschr. zum GOten Geburtst. Hi>rtwigs,
vol. 1, 1910.

Biitschli. Zur Entwicklungsgeschiehte der Sagitta,. Zeitsclir. "Wiss. Zool., vol.
23, 1873.

Doncaster, L. On the Development of Sagitta, with Notes on the Anatomy of the
Adult. Quart. Journ. Micr. Sc. , vol. 46, 1902.

Giinther, R. The Chaetognatha or Primitive Mollusca. Ibid., vol. 51, 1907.

Hertwig, O. Die Chaetognathen. Jena Zeit, vol. 14, 1880.

Kowalevsky. Embryologische Studien an Wiirmern und Arthropoden. Mem.
Acad. Petersbourg, 7th series, vol. 16, 1871.

CHAPTER XV

NEMATODA

THE Nematoda, often called Thread-worms or Eound-worms, are a
group in which there is wide diversity of habitat and life-history,
but most remarkable uniformity in adult structure. The vast
majority are parasitic during some period of their existence ; it is
indeed by no means certain that even among the so-called free-living
Nematodes many have not a parasitic stage in their life -history,
because this history is very far from being completely known.
Though they infest the most diverse animals and plants, the
structure of the young worm, before the genital organs are developed,
is remarkably constant throughout the group ; and so is the embry-
onic development so far as it is known. Owing to the fact that the
eggs and embryos are very minute, the method of sections has been
hardly at all applied to the study of the group ; most observations
have been made on the living embryo seen through the semi-
transparent egg-shell, whilst others have been made on embryos
fixed, stained, and mounted whole.

In spite, therefore, of numerous investigations, much remains
obscure in the embryology of these worms. Indeed it must be said
that most of these investigations have had for their object the solution
of general problems, such as the relative importance of cytoplasm
and nucleus in heredity, the relationship of genital and somatic cells,
the nature of the polar bodies, etc., rather than the elucidation of
the special course which development takes in this group, and the
light which it throws on the affinities of the group. These words
are not said to disparage the painfully laborious investigations
which have already been made, but to indicate that there is still a
promising field left for future investigators.

ASCARIS MEGALOCEPHALA

The form whose study lias so far yielded the most satisfactory
results is Ascaris megalocephala, a large ISTematode, about 9 or 10
inches long, which inhabits the intestine of the horse and causes no

437

438 INVERTEBRATA CHAP.

noticeable ill effects. It is readily obtained in great numbers at
the abattoirs.

The eggs are contained in the two uteri. They do not commence
to develop until they have been laid, but once they have commenced
to develop they are wonderfully tenacious of life. If they are spread
on slides and attached to the slide with albumen fixative, and the
slides are then put into a moist chamber or even into weak formalin,
their vitality is quite unimpaired and they pursue an orderly course
of development. This can be suspended by exposing them to cold,
and when the temperature rises the development is resumed at the
point at which it left off. This circumstance makes the development
of Ascaris an extremely convenient subject to work at for a professor
burdened with professional duties ; when he has leisure the develop-
ment is allowed to proceed, when he is busy with other duties the
development is suspended by exposing the eggs to cold.

A word or two on the adult anatomy might be in place here.
It is characteristic of most Nematoda to have two female organs,
which open by a pore situated on the mid-ventral line about one-
third the length of the body from the front end. Each of these
organs consists of a long tube. The distal end of this tube is
practically solid and contains large nuclei embedded in a mass of
cytoplasm, in which cell divisions are not obvious. As one proceeds
i'arther down the tube a cavity appears, and the cytoplasmic
territories of the various nuclei become delimited from each other
so that we can speak of a layer of cells surrounding a cavity.

These two sections of the tube are known as the ovary. Below
this the ova become detached from the lining of the tube and lie
in its cavity. This portion is termed the oviduct. Here the
maturation divisions take place and the male cells meet and unite
with the female cells. Below this the tube widens and the eggs
become surrounded by their horny egg-shells, in which they
complete most of their development. This section is termed the
uterus. Finally there is an extremely short terminal piece common
to the two tubes and known as the vagina.

The sexes are separate in Ascaris megalocephala as in the great
majority of ISTematoda. The male organ consists of a single tube
which, in a manner similar to the topography employed in the case
of the female organs, is mapped out into a testis, without cavity
and with undivided cytoplasm and numerous nuclei, a hollow vas
deferens, in which the male cells become detached and mature, and
a terminal vesicula seminalis in which the mature male cells are
stored up. This tube opens near the posterior end into an ectodermal
pit or atrium, the cloaca, into which the posterior end of the
alimentary canal also opens.

Two horny spicules, inserted in ectodermal pockets of the cloaca at
the sides of the male genital opening and capable of being extruded by
special muscles, are used to distend the genital opening of the female
and effect fertilization. These are known as copulatory spicules.

XV

NEMATODA 439

The male cells of Nernatoda are not spermatozoa but small
amoeboid cells with large nuclei. By carefully opening mature
specimens of Ascaris megalocephala and unravelling the genital tubes
so gently as not to break or injure them, by then carefully dividing
these tubes into short lengths which are numbered so as to show
the position of each portion in the tube from which it was taken, and
by preserving these portions in separate bottles, material may be
obtained for an exhaustive study of the maturation of male and
female cells, and it was in this way that Hertwig in 1890 obtained
evidence as to the nature of the polar bodies.

It is a most remarkable fact that there are two races of Ascaris
megalocephala,, in one of which there are four chromosomes in the
oogouia and spermatogonia, and two chromosomes in the ripe eggs
and male cells; and in the other of which there are two chromo-
somes in the oogonia and spermatogonia, and one chromosome only
in the nucleus of the ripe eggs and male cells. The first variety is
called livalens, the second monovalens. The genital cells at any
given cross section of the genital tube are all in the same stage of
development.

The most exhaustive studies of the development of the fertilized
egg have been made by Zur Strassen (1896) and by Boveri (1899), who
observed the development up to about the 200 -cell stage, also by
the 'former's pupil Milller (1903), who endeavoured to carry on the
analysis of the development up till the time when the young worm
was hatched.

Zur Strassen's method of making whole mounts of the eggs and
embryos was as follows. The eggs were fixed by being placed for
twenty-four hours in a mixture of four parts of 95 per cent alcohol
and one part glacial acetic acid ; they were then stained for
twenty -four hours in Grenadier's hydrochloric acid carmine; the
excess of stain was removed by immersion for forty-five minutes in
95 per cent alcohol to which I per cent of hydrochloric acid had
been added. They were then washed in 95 per cent alcohol. Some
glycerine was added to this, and by allowing the alcohol to evaporate
gradually the eggs were got into a solution of pure glycerine. The
eggs were examined in this medium, and by gently pressing on the
coverslip they could be rolled into various positions and examined
from all sides. Boveri recommends similar methods, but he also
employed picro-acetic acid, made by adding to a concentrated solution
of picric acid in water, two volumes of water and 1 per cent of
glacial acetic acid.

The segmentation of the egg of Ascaris megalocephala is by far
the most specialized development that has ever been described.
Many workers besides Zur Strassen have examined it, and a nomen-
clature has been gradually agreed on, which will be employed here.
This nomenclature was not fully developed when Ziir Strassen wrote
his long descriptive paper, but it is easy to translate the nomenclature
which he there employs into the more modern nomenclature.

440

INVERTEBRATA

CHAP.

The egg divides into two blastomeres, an upper and a lower.
The upper, which is designated AB, is slightly larger and freer from
yolk granules than the lower, which is designated Pr The nucleus
of AB undergoes an extraordinary change known as the " diminution
of the chromatin " (Fig. 342, B). At the moment that it separates
from its sister nucleus in Px, it contains, like the fertilized egg, four
chromosomes (or two in the variety monovalens). But as it passes
into the resting stage, the greater portion of each of these chromosomes
is cast out as amorphous masses of chromatin, which for a time can
be recognized in the cytoplasm but which are gradually absorbed.

The remainder of each chromo-
some breaks up into a number of
minute granules.

When AB next divides each
of these granules acts like a
minute chromosome, and hence
the spindle that is formed ex-
hibits a totally different appear-
ance from the spindle that is
formed in P]; which shows, of
course, the ordinary four (or two)
chromosomes.

At the next cleavage AB
divides into an anterior cell A
and a posterior cell B, whilst Pt
divides into an upper cell de-
nominated EMST and a lower

FIG. 342.— The 2-cell stage of the egg of
Ascaris megalocephala (monovalens) when
the spindles for the 4-cell stage are being
formed, showing diminution of the chroma-
tin. (After Boveri.)

A, the 2-cell stage seen from the side. B, two
chromosomes from the upper cell enlarged to show
the process of diminution of the chromatin.

cell P2. The nucleus in EMST

undergoes a reduction precisely
similar to that undergone by the
nucleus in AB. The embryo is
now shaped like a T. The two
lower cells bend upwards first in
a plane at right angles to the plane of the two upper cells ; they
then, however, swing round into the same plane, and so the T becomes
a rhomb, find the plane of this rhomb is the future median plane
of the embryo.

At the next cleavage A divides into a right cell named a and a
left cell named a. B divides similarly into a right cell named b and
a left cell named (3. EMST divides into an anterior cell named
MST and a posterior one named E. P2 divides into an anterior cell
called P3 and a posterior one called C. The nucleus in G undergoes
reduction so that only P3 retains large chromosomes. The four cells
MST, E, P3, and C follow each other in a curve, convex below, which
lies in the median plane of the embryo. They and their descendants
are known as the ventral cell family, whilst a, b, a, and ft, and
their descendants, are known as the dorsal cell family.

The dorsal cell family divides much more rapidly than the

XV

NEMATODA

441

ventral cell family, but befure any further divisions take place certain
characteristic rearrangements of the members of the dorsal family
occur. On the right side a glides upwards and & downwards, whilst
on the left side a glides downwards and (3 upwards (Fig. 343, D).

At the next cleavage all four cells divide and the two daughters
of each are denominated 1 and 2, the more dorsal sister being indicated

B

EMST

ST

FIG. 343. — Early stages in the segmentation of the egg of Ascuri.<t megalocephala.

(After Boveri.)

A, 4 -cell stage in the T • condition seen from the right side. B, 4 - cell stage in the rhomb
condition seen from the right side. C, 6-cell stage seen from the right side. 1>, s-rell sl.-i-r seen
from the right side.

by the suffix (1). As a result of the gliding that has taken place in
the previous stage, the four cells of the upper cell family on the right
side form a T-piece with a horizontal beam and a vertical cross-piece.
The beam consists of 51 in front and &., behind, the cross-piece of ax
above and a.2 below. The four cells on the left side form a rhomb «,
and a.2, lying rather in front of, but beneath, /^ and fi.,. The four
cells of the ventral cell family form a horse-shoe with approximated
ends. Then a fresh rearrangement takes place, ^ passes to the

442

INVERTEBRATA

CHAP.

middle line between c and «9 ; « is below and in front, whilst ax is

9

above and behind ; the effect of this is to force apart the limbs of the.
horse-shoe formed by the ventral cell family and to force the terminal
cell C backwards and downwards (Fig. 344). A new T-piece is then

Fl«. 344. — The 12-cell stage of the .segmentation of the egg of Afn'un'.-i iii<'<i<t/<i<-<'j>lnil<i,
seen from the left and the right sides respectively in order to show the rearrangement
of the daughters of the cell AB. (After Zur Strassen. )

A, from the left .side. B, from the right side. The daughters of A have the lightest tone. Those of B
have the same tone crossed with oblique lines. The ventral cell family have the deepest tone.

formed, which persists throughout the whole development. The cross-
piece of this T is horizontal and is made by the two cells az and a.7,
the beam is constituted by the two cells «x and a, (Fig. 345).

err

FIG. 345. — Dorsal view of the segmenting
egg of Ascaris megalocephala in the
20-cell stage. (After Zur Strassen.)

FIG. 346. — Ventral view of the segmenting
egg of Ascaris megalocephala in the 24-

cell stage. (After Zur Strassen.)

In this stage the embryo is an egg-shaped blastula.

Then the cells of the ventral cell family divide. MST divides into

;i right cell denominated mst, and a left one denominated

E

divides into Ex in front and E2 behind, P3 divides into P4 in front
and D behind, and C divides into a right cell c and a left cell y.

NEMATODA

443

The nucleus of D undergoes reduction of chromatin, so that finally
only the cell P4 is left in which the chromosomes retain their original
condition. This cell in the subsequent development divides only
once until the larval period is attained, and it is the parent cell of
the genital organs and gives rise to nothing else.

It follows, therefore, that the tissues of the Nematode are con-
structed of cells which have lost a large part of the chromatin which
they had inherited from the egg cell, and which are, therefore, as
compared with the germ mother cell, degenerate cells.

Zur Strassen has followed in detail the subsequent divisions of
the dorsal cell family, adopting for his purpose a most complicated
nomenclature, but nothing is gained by following him because there
is some evidence to show
that these cells are
equivalent to each other,
and that if, through
abnormal circumstances,
their number is increased,
it does not affect the
normal development of
the resulting embryo.
The daughters of A, as
we have seen, form a
median T -piece, and the
two sides of the beam of
this are occupied by the
daughters of b and ft
respectively.

Zur Strassen's object
was to discover if the
mutual displacements of
the cells of this family
could be accounted for
by the laws of surface-
tension, or whether there was evidence of cytotaxis, i.e. mutual
attractions and repulsions of cells based on their chemical qualities.
He found that surface-tension did undoubtedly cause rearrangement ;
it caused the cells to arrange themselves according to Plateau's
principle, i.e. in such a way that the total area of their boundary
surfaces was reduced to a minimum ; but he also found that it was
not the sole principle at work, because in some cases cells moved in
such a way as to directly contravene that principle, and hence there
was evidence that cytotaxis was at work (Fig. 347).

Returning to the last stage minutely described, when both dorsal
family and ventral family consisted of eight cells, i.e. the 16-
cell stage, we may note that at this stage the egg forms an elliptical
blastula with a well-marked blastocoele. The first trace of the
iuvaginatiou which will change the blastula into a gastrula is seen

FIG. 347. — Dorsal view of the segmenting egg of Ascaris
megalocephala in the 102-cell stage. (After Zur
Strassen.)

The daughters of A forming the permanent cross are light-
coloured. Those of '/ and j3 are cross-hatched.

444

INVEETEBKATA

CHAP.

D

in the cell E, which is the mother cell of the endoderm. Before this
cell divides into Ex and E2 the nucleus shows a tendency to migrate
inwards and upwards, but when it divides the daughter nuclei lie at
the ordinary level.

At the next division of the cells of the ventral family, mst divides
into an anterior cell st, which is one of the cells which form the
stomodaeum, and a posterior and lateral cell which is one of the
mother cells of the anterior mesoderm. /MTT similarly divides into
a stomodaeal cell O-T and a niesoderm mother cell p. (Fig. 346). Ej and
E2 divide into right and left daughters which (following Plateau's
principle) assume a rhombic arrangement. The two tail cells c and y
each divide into an anterior and a posterior cell, and the cell D also
divides into right and left daughters. The nuclei of all four en-
doderm cells take up posi-
tions near the inner margin
of their respective cells, the
cytoplasm follows suit, and
so the process of gastrula-
tion is initiated (Fig. 348).
In the next stage P4
divides into an anterior
Gl and a posterior G2.
These two cells remain
quiescent and undergo no
further division until after
the larva is hatched and
the development of the
genital organs is begun.
Boveri, however, maintains
that sometimes, at any
rate, the hinder of these
cells divides into right and
left daughters which are
ectoderrnal, and that the two mother germ cells arise by a second
division of the front cell. The anterior pair of tail cells divide each
into two daughters lying side by side, so that a transverse row of
four is formed, but the posterior tail cells divide each into two, one
behind the other. The stomodaeal cells each divide into anterior and
posterior daughter cells, and slightly later the anterior niesoderm
cells follow suit. These mesoderm cells now pass into the blastocoele
and lie between ectoderm and endoderm on each side (Fig. 351).

In the next cleavage both stomodaeal cells and mesoderm cells
are raised to four on each side. In this way two short mesodermal
bands are formed, each consisting of four cells, but each band
contracts so as to form a rhomb. The endoderm cells increase
to eight. The daughters of D (d and S) divide each into two cells,
lying side by side, so as to form a transverse line of four cells parallel
to the row formed by the front tail cells.

FIG. 348. — Optical median sagittal section through
the blastula of Ascaris megalocephala at the time
that the process of gastrulation is commencing.
(After Boveri.)

The cells P4 and D are beginning to extend beneath E2.

XV

NEMATODA

445

Next, the second pair of stomodaeal cells come into contact with
each other, the first pair are in contact from their first formation,
and this group of four sinks inwards. Of the posterior group of the
tail cells each divides into anterior and posterior daughters, and in
this way a double row of eight is formed (i.e. four pairs, one behind
the other). Each transverse row of four, i.e. the row formed from
the front tail cells and the one formed from D, folds up into a
U -shape. The hinder U merely continues the line of the tail cells,
but the front one sinks inwards and forms, as Miiller has asserted,

U

FIG. 349. — Segmenting egg of ASCII ri-x •iiit'i/n/ixr/ilinht, in the 10'2-cell stage seen from

beneath. (After Miiller.)

All the ectoderm cells which are descendants of AB have a light tone — the descendants of A and
those of B are not distinguished from one another, lilp, blastopore. u, the front row of tail cells
descendants of C, which bend up so as to form a U. A similar U in front of this one is formed by the
descendants of U (dj, do, Si, &-J and gives rise to mesoderm.

a posterior mesoderm rudiment. (Zur Strassen had imagined that
it gave rise to the proctodaeum, but this is an error.) Miiller further
asserts that a third mesoderm rudiment is formed, at a later stage,
from some of the tail cells (Fig. 349).

Zur Strassen maintains that the tail cells, the descendants of C,
are distinguishable from the descendants of AB, which he denominates
the primary ectoderm, by their clearer protoplasm and flatter shape ;
and he maintains that, as development proceeds, the tail cells pro-
gressively displace the primary ectoderm cells till these last form
only a small cap at the anterior end of the embryonic worm. Miiller,
however, has not been able to confirm this. The blastopore closes

446

INVERTEBRATA

CHAP.

by the gradual approximation of its sides, and it is for a brief period
long and slit-like (Figs. 350, 351).

en

d a

stom

end

slam

FIG. 350. — Median sagittal sections through three eml>ryos of Ascaris megalocephala, iii order
to show the invagination of the genital cells and of the stomodaeal rudiment. (After Boveri.)

A, embryo at the close of gastrulation ; a. small part of the endoderm is still uncovered. B,
embryo in which gastrulation is complete : the stomodaeal cells begin to be invaginated. C, embryo
in which tin- stomodaeal cells form a tube, and in which the mother cells of the genital organs are
covered in by ectoderm, hip, blastopore ; end, endoderm ; stout, stoinodaeuin.

As the tail cells multiply and the embryo elongates, a remarkable
rearrangement takes place in some of the ectoderm cells covering

XV

NEMATODA

447

the dorsal surface. These at first form two rows interdigitating
with each other, but they quickly rearrange themselves so as to form
a single row of band-like cells. Miiller has observed two large clear
cells lying on the ventral surface in the anterior part of the animal.
These he surmises to be the mother cells of the excretory tubes.
Although these tubes extend in the adult through nearly the entire
length of the animal, they are each composed of a single hollowed-
out cell.

mes

gen

gen

FIG. 351. — Transverse sections of embryo of A scans megalocephala, in order to show the
imagination of the anterior mesoderm cells and of the mother cells of the genital organs.
(After Boveri.)

A, section of a stage in which the eniloilerm cells art- invaginated, but in which I in' mesoclei \\\ cells
are still superficial. B, section of a stage in which the mesoderm cells have passed into the blast <>•
coelic cavity. C, section of a stage in which the genital cells are beginning to be inviigiiiated. D,
section of a stage in which the invagination of the genital cells is complete.

When the young worm finally hatches out — which, under normal
circumstances, must occur amongst the horse-dung which has been
dropped on the ground --it is known as a Rhabditis larva, and
it only becomes converted into a mature worm after it has been
swallowed by a horse.

The reader will not fail to observe what large gaps there are
in the account of the development which has just been given, and
what a field there is for future work. The problem of tracing the

fn.es

448 INVERTEBEATA CHAP.

embryonic rudiments into the larval organs has been most imperfectly
accomplished, and it is quite obvious that before much more progress
is made in this direction the method of whole mounts will require
to be supplemented by that of sections, and some means must be
devised for getting the embryos out of the egg-shell.

EXPERIMENTAL EMBRYOLOGY OF NEMATODA

Zur Strasseu's descriptive paper, long as it is, pales into insig-
nificance beside his paper on the " T-Giants " (1906). These T-Giants
are abnormal embryos produced by the fusion of unfertilized eggs.
This fusion occurs only in a very few cases in any one individual,
and it is the more apt to occur if the individual is subjected to
extreme cold. The eggs first of all cohere, then at the points of
contact the egg-shells become softened and finally absorbed, and
then their protoplasmic contents are free to coalesce. In this way a
multinucleated mass is formed, but usually only one male cell enters
it and only one of the egg-nuclei is fertilized ; the others degnerate.
As a result, an abnormally large egg is formed, and occasionally,
if the shape of the egg-shell resulting from the coalescence of
several egg-shells is suitable, this large egg may develop into a
perfectly normal large embryo.

But in many cases the composite shell is long and narrow, -not
spherical in shape. Consequently, when the contained composite egg
has divided into four and taken on the form of a T (whence the
name T-giant), and when in the normal course of things the cell C,
which forms the lowest part of the beam of this T, should swing
upwards and come into contact with B, the narrowness of the shell
prevents it doing so ; and after much writhing, which bears witness
to the reality of the forces denominated cytotaxis, the cell C settles
down to continue its development in its abnormal position.

The life of a T-giant is, however, of very limited duration. The
descendants of AB (the dorsal cell family) divide repeatedly, so as
to form an irregular vesicle of cells, the ventral cell family carry
out several divisions, but soon granular degeneration sets in and the
embryo dies. In one case, however, after the first division in the
ventral cell family had taken place, the whole embryo had so con-
tracted that it was now possible for C to swing upwards; but this
swing upwards took place to the left instead of, as in the normal
embryo, in the median plane, and as a consequence C became wedged
in between a and /3 instead of between b and ft, as it should have
done. Nevertheless, in the further development of this embryo
considerable readjustment took place. Although at first the cells
of the ventral cell family occupied abnormal positions (mst, for
instance, being in front of /^O-T), yet they glided on each other
till the normal position was very nearly attained, and, indeed, the
embryo showed every sign of developing into a normal larva until
it met its death by an accident. In this case it seems as if the

XV

NEMATODA

449

e.m

abnormal relation of the ventral cell family to the descendants of
AB had not seriously affected the development.

Zur Strassen's object in the special study of these T-giants was
to elucidate the proximate causes of the orderly succession of all
divisions and the orderly movements of the cells on one another, to
which the definite form of the body of the embryo owes its origin.
Since, even in a T-giant, for instance, C divides evenly into c and y,
which lie side by side where C is widely separated from contact with
b and f3, it is obvious that the direction of the spindle in this
division is in no way influenced, even in the normal embryo, by the
neighbourhood of b and /3 to C.
To a certain extent the cell C is
self-differentiating, i.e. it has the
causes of its development within
itself, and the question arises
whether these causes lie in the
cytoplasm or in the nucleus.

Zur Strassen decides that the
causes must lie in the cytoplasm,
because the nucleus, both in the
resting stage and in the prophases
of karyokinesis, is seen to rotate
so as to reach its definite position,
like a body swept along by a
current. The cause he imagines
to be an invisible differentiation
of the cytoplasm in a definite
direction, so that we may conceive
its material to be arranged in a
series of parallel planes like the
cleavage planes of a crystal.
These planes, he imagines, com-
pel the spindles of the dividing
nuclei to be built up either
along them or at right angles to

them, and in turn we might suppose that the planes owed their
existence to the effects left on the cytoplasm by the previous spindle.

If we do so, Zur Strassen shows, by most acute reasoning, that we
are driven back step by step till we have to assume that these planes
existed in the fertilized egg. The cytoplasm of the fertilized egg
would, on this assumption, be of a most complex constitution. Zur
Strassen assumes the existence of three sets of cleavage planes at
right angles to each other, as well as of several sets of oblique planes,
and there is the possibility that this hypothetical constitution would
not suffice if he were to carry his analysis of the development to a
later stage.

In order to account for the movements of the cells on one
another, which are just as important as the directions of the spindles

VOL. I 2 G

FKJ. 352. — A "T-giant" of Ascaris megalo-
' cephala seen from the left side. (After
Zur Strassen.)

ect, ectoderm cells descendants of AB; e.m, egg-
mem bran c.

450

INVEETEBRATA

CHAP.

in determining the form of the embryo, Zur Strassen imagines that
these planes are the seats of some sort of attraction which tends to
cause similar planes in other cells to set themselves parallel with
them. Further, he imagines that this attraction can wax and wane
with the physiological condition of the cell, and by a climax of
ingenuity he endeavours to account for the swinging round of the
beam of the T, first to the left and then into the middle line, by the
successive attraction which two sets of planes at right angles to each
other, in the cells A and B, exercise on the planes in the lower cell.
The question then arises whether these planes exist in the

A

B

EMST

FIG. 353. — Two diagrams of the 4-cell stage in the development of the egg of Ascaris
megulocephala, in order to show the cytoplasmic zones which Zur Strassen assumes to
exist in the blastomeres. A, the T condition. B, the rhomb condition.

One set of planes is indicated by broad bands, another by thin lines. The broad bands in the
upper cells first attract the thin lines in the lower cells, and ¥% swings up at right angles to the paper,
so that the bands in the upper cells and the lines in the lower are parallel to one another ; then the
bauds in the lower cells are attracted by the bands on the upper cells, and set themselves parallel to
thesi1, and so the condition shown in B is attained.

unfertilized egg or are formed after fertilization. It occasionally
happens that a giant egg is doubly fertilized and gives rise to twins.
The axes of these twins are often divergent, and sometimes one is
much bigger than the other. Hence we have to assume the exist-
ences of two complete sets of the hypothetical planes, and to further
assume that each set extends through a different region of the cyto-
plasm. The only way out of the difficulty, according to Zur Strassen,
is to assume that the planes are manufactured in the cytoplasm ly
influences emanating from the zyyote nucleus.

For this assumption there is corroborative evidence afforded by
the development of other forms ; for instance, in the development of

xv NEMATODA 451

Dentalium (see p. 325) and still more strongly in the development of
the simple Ascidians as worked out by Conklin. If the objection be
raised that it is hard to see why if the zygote nucleus has such a
profound effect on the cytoplasm its daughter nuclei should not have
an equal effect, it must be answered that there is definite evidence in
Echinoderni development that they do not have any effect, that, in
fact, coiucidently with the entrance of the spermatozoon and the union
of the two sexual nuclei, a rearrangement of substance takes place
which has no parallel in later development. It is suspected that the
separation of ectoderm, endodcrm, and mesoderm, which forms the
first step in development, the so-called "formation of layers," may Jind
its cause in this rearrangement of cytoplasmic material ; and the well-
known circumstance that bud development does not follow the lines
of embryonic development (vide Chaps. XI., XVII.) may be due to the
fact that the nuclei of a bud-rudiment revert to the zygotic condition
and rearrange the surrounding cytoplasm but in a different manner.

Whether Zur Strassen's explanations are justified in detail or not,
which is very doubtful, it is difficult to escape the cogency of his
reasoning that some such differentiation must exist, even in appar-
ently homogeneous cytoplasm, in order to account for the direction of
spindles and the movements of cells ; unless we are going to have
recourse to an imaginary indwelling spirit, the Entelechy of Driesch,
to account for these things.

Boveri (1910) has\also made investigations on the abnormal
embryos of Ascaris, but' the type of abnormality which he has chosen
to investigate is different from that to which Zur Strassen has devoted
his attention. Boveri has chosen for his special subject doubly
fertilized eggs. These are to be found in small numbers in almost
every lot of Ascaris eggs submitted to investigation. They are
recognized by the fact that at the first cleavage they divide into four
equal cells. One of the male nuclei fuses with the female nucleus,
and as usual brings in its own " cytocentre " or centrosome, and the
other male nucleus forms an independent cytocentre, so that at the
first division four cytocentres are formed and the egg divides into
four cells.

Now Boveri has proved that there are three varieties of these
doubly fertilized embryos. In one variety one of the four cells acts
as F, and in subsequent cleavages gives rise to a perfectly normal
ventral cell family, whilst the other three act as AB's, and each
divides as the upper cell in a rlbrmal egg would have done (Fig.
354, A). The product of all three coalesce to form a much too
voluminous cell cap of " primary ectoderm," but there are indications
that embryos of this type occasionally give rise to normal larvae.

In the second variety two of the four cells act as F's, and two
as AB's. The result is the production of a "parallel twin" (Fig.
354, B). Development goes on for a certain distance, but the two
ventral cell families interfere with each other's expansion, an
irregular mass of cells results, and then death supervenes.

452

INVERTEBRATA

CHAP.

In the third variety only one of the cells functions as AB, the
other three act as P's (Fig. 354, C). The three ventral cell families
which result become intertwined with one another in the most varied
manner. Some cells eventually become detached from one and added
to another, and eventually the irregular mass of cells which results dies.

Boveri accounts for the occurrence of these three types of embryo
by assuming that the diminution of the chromatin which differentiates

EMST

AB

EMST

FIG. 354. — The stage corresponding to the 4 -cell stage in the development of the normal
egg, which occurs in the development of the three types of doubly fertilized eggs of
Ascaris megalocephala. (After Boveri.)

A, egg in which three dorsal cell families and one ventral cell family develop. B, egg in which two
dorsal cell families and two ventral cell families develop. C, egg in which one dorsal cell family and
three ventral cell families develop.

AB from P is determined by the presence or absence of some peculiar
cytoplasmic substance in part of the egg cell, or rather by its presence
in greater amount in one place rather than in another. When three
AB's and one P are formed, three of the cytocentres are situated in
the region which determines diminution and one in the other region ;
when three P's and one AB are formed, one of the cytocentres is
situated in the region causing diminution and three elsewhere ; and,
finally, when two AB's are formed, two cytocentres are situated in this
region.

NEMATODA

453

MST

In these doubly fertilized eggs a complex spindle is formed con-
necting all four centres in the most varied and complex ways, and on
the parts of this spindle the various chromosomes, derived from the
ovum and from the two male cells, are distributed in the most
irregular fashion. Boveri, from a collection of suitable cases, shows
that the assumption that the process of diminution is a thing deter-
mined by the specific character of some of the chromosomes leads to
perfectly untenable positions. The conclusion, therefore, that the
cause of diminution lies in the cytoplasm is unavoidable.

This conclusion is confirmed by the results of some remarkable
experiments which Boveri carried out on the normal eggs of Ascaris.
When these eggs are subjected to the action of severe centrifugal
force (about 3000 revolutions per
minute), and when the axis of sym-
metry of the egg is placed perpen-
dicularly to the axis of rotation, then
the first cleavage spindle, instead of
lying in the axis of the egg, is situated
at right angles to it. i.e. tangentially to
the direction of rotation, and the egg
divides into two precisely equal cells,
each of which acts as a P and gives
rise to a ventral cell family. The eggs
which thus gave rise to two ventral
cell families were termed by Boveri
"ball-eggs," because a peculiar

sphere of granular material, devoid FIG. 355.— stage in the development
of a nucleus, was found to be ejected
from the egg in the direction of a
radius of circle of rotation (ej, Fig.
355). If the axis of the egg lies
obliquely to the axis of rotation, then

the first division, even after violent centrifugal action, gives rise to
P and AB cells as usual.

It follows that, when the peculiar diminution-causing substance
is symmetrically distributed with regard to the first spindle, no
diminution results, but that when one side of the egg gets a little
more than the other, diminution occurs in one of the two daughter
nuclei.

That the peculiar development of P and AB is in each case due
to the peculiarity of the cytoplasm in each of the two cells, and is
not due to the mutual reactions of these cells, is proved by another
ingenious experiment of Boveri. A large number of developing
Ascaris eggs were spread on a slide and covered with a coverslip.
On the coverslip a large number of parallel narrow bands of tin-
foil were fixed a very short distance apart. When the eggs had
reached the 2-cell stage the slide was brightly illuminated by a
mercury vapour lamp, the light of which contains a large proportion

of a "ball-egg" of Ascaris inegalo-
cephala corresponding to the 8-cell
stage in the development of a
normal egg. (After Boveri. )

ej, ejected mass of granular material.

454 INVERTEBKATA CHAP.

of ultra-violet rays. These rays kill all the cells they reach, but it
often occurred that one cell of a 2 - cell embryo was exposed to
the light whilst the other was sheltered by the tin-foil. In this
way it could be shown that when P is killed AB develops into a
closed vesicle of similar cells, and that when AB is killed P gives rise
to a typical ventral cell family just as it does in the uninjured egg.

Another most interesting result was obtained by centrifuging the
unfertilized eggs. These, under the stress of strong centrifugal force,
throw off parts of their substance, so that their volume is often
diminished by one-half, and yet when subsequently fertilized they
give rise to perfectly normal embryos of correspondingly reduced
size.

The conclusion is therefore obvious, that the cytoplasm of the un-
fertilized egg is homogeneous, and that its differentiation into definite
regions only takes place at fertilization, and thus, in a different way,
Boveri arrives at exactly the same conclusion as that which Zur
Strassen had already reached.

The points sought to be elucidated by Zur Strassen's and Boveri's
researches are thus seen to be general questions bearing upon the
nature and mechanism of development in general.

The embryonic development of other Nematoda, so far as is
known, agrees closely with that of Ascaris and ends in the develop-
ment of a similar Rhabditis larva. The larval development varies
enormously according to the condition under which the larval life is
passed and the animal or plant in which final ripening takes place ;
but the study of these life-histories lies outside the scope of this book.

AFFINITIES OF NEMATODA

Before concluding, a few words on the question of the affinities of
the Nematoda may be in place. On this question the development
throws practically no light at all. Of course, in a general way, it
may be said that a hollow blastula is formed and that a gastrula
arises by invagination ; but the blastomeres are specialized at an
unprecedentedly early stage, and yet their specialization is very
different from that observed in eggs with spiral cleavage, which are
the only other cases where anything like such early specialization is
known to occur. Moreover, our knowledge of the complete develop-
ment is so faulty that we cannot as yet make profitable comparisons.
Zur Strasseu asserted the existence of a single niesodermic rudiment
on each side which, at a stretch, might be compared to a niesodermic
band ; but his pupil, Mliller, asserts that the mesoderm arises from
three distinct sources, viz. from MST, from D, and from the most
anterior daughters of C.

A thorough and exhaustive revision of the normal development
is the first pre-requisite for any profitable theorizing on the subject.

On grounds of comparative anatomy a relationship with the
Chaetognatha has been suggested. Both groups have a strong

xv NEMATODA 455

tendency to produce cuticle, both have a simple, straight alimentary
canal devoid of appendages, and both possess a single layer of
longitudinal muscles and no circular muscles. The excretory organ
of Chaetognatha must be regarded as the coeloinic cavity. This is
suppressed in Nematoda, but a similar phenomenon is seen in
Arthropoda, which are undoubtedly derived from the coeloniate
Annelida, and the suppression of the coelomic cavity may be con-
nected with the excessive production of cuticle. The excretory cells
of Nematoda have no known homologues in Chaetognatha and the
early development is very dissimilar. That of Chaetognatha is of a
very primitive type, whilst that of Nematoda is excessively specialized.
In one feature alone do they resemble one another, i.e. in the early
differentiation of the genital cells.

Perhaps a more thorough knowledge of the normal development
of Nematoda would enable us to regard it as a modification of that
of Chaetognatha, but for the present the question must be left in
abeyance.

LITERATURE REFERRED TO

Boveri, Th. Die Entwicklung von Ascaris megaloccphala niit besonderer Riicksicht
auf die Kernverha'ltnisse. Festschrift zuni 70ten Geburtstag von Carl von KupflV-r.
Jena, 1899.

Boveri, Th. Die Potenzen der ^scaHs-Blastomeren bei abgeanderter Forderung.
Festschrift zum GOten Geburtstag Richard Hertwigs. Jena, vol. 3, 1910.

Hertwig, O. Vergleich der Ei- und Samenbildung bei Nematoden. Archiv fur
mikroscopische Anatomic, vol. 36, 1890.

Miiller. Beitrag zur Embryonalentwicklung der Ascaris megaloccphala. Zoologica,
Heft 17. Stuttgart, 1903.

Zur Strassen. Embryonalentwicklung der Ascaris megalocephala. Archiv fur
Entwioklimgsmechanik, vol. 3, 1896.

Zur Strassen. Die Ueschichte der T-Riesen von Ascaris megaloccphala. Zoologica,
Heft 60. Stuttgart, 1906.

CHAPTER XVI
ECHINODERMATA

Classification adopted—

Asteroidea
Ophiuroidea

fAsteroidea

. ,
Eleutnerozoa- ' , . .,

Ecninoidea

^

Holothuroidea
[Blastoidea (Extinct)

Pelmatozoa °Ptoi*ea ^^
Thecoidea (Extinct)

Crinoidea

THE Echinodermata, as they at present exist, are divided into five
very distinct classes of animals, viz. Asteroidea, Ophiuroidea,
Echinoidea, Holothuroidea, and Crinoidea. The first four of these
classes agree in possessing the power of free locomotion during the
adult stage ; and, when a fixed stage does occur in the course of
development, the fixing organ is attached to the oral surface of the
animal. For this reason the four classes mentioned are grouped
together in a sub-phylum termed Eleutherozoa. The members of
the fifth class, Crinoidea, possess at some time of their existence a
fixing organ situated at the aboral pole of the body, and this organ
is retained by many of them throughout life; for this reason the
Crinoidea, together with some extinct classes of Echiuoderniata, are
grouped together as Pelmatozoa.

In three of the four classes of Eleutherozoa the development of
one species has been worked out in great detail, and in the case of
the fourth class, although many points are still obscure, the general
course of the development is well known. The development of only
one Pelinatozoon is known, and in this case a large part of the
development is passed through within the egg-membrane ; whereas
the corresponding stages of development in Eleutherozoa are passed
through in the free larval condition.

A great deal of experimental work has been done on the eggs and
larvae of Echiuodermata, and most important results have been
obtained which differ in many points from the results obtained from

456

CHAP, xvi ECHINODEKMATA 457

experiments on the eggs of those groups of animals (cf. Coelenterata,
Nemertinea, Mollusca, and Nematoda), which we have already
discussed. For this reason it is necessary that the normal course of
development in Echinodermata should be described in detail.

Of the four groups of Eleutherozoa, the one which presents the
most primitive features in its development is the Asteroidea, and we
shall commence our study of the development of Echinodermata by a
consideration of this group.

ASTEKOIDEA

In a few cases the entire development of an Asteroid has been
worked out, and the manner in which the organs of the adult are
fashioned out of the body of the larva has been elucidated. The
species which have been thus studied are Asterina gibbosa, Cribrella
oculata, and Solaster endeca. Unfortunately in all these cases we
have to deal with an egg which contains a good deal of yolk, and
with a development which is much moditied and hurried on.
Asterina gibbosa is the least modified of the three, for its larva
possesses a mouth and it can take food in the larval condition,
whereas in the case of the other two species the gut is delayed in its
development, and the larva possesses no mouth.

In the more normal type of development, such as is met with in
the genera Asterias, Astropecten, Luidia, etc., the egg develops into a
larva which possesses a complete alimentary canal, and lives a free-
swimming and self-supporting life for a long period, often extending
over two months, until at last it metamorphoses into the adult form.
The eggs of several species of Asterias have been successfully reared
through the metamorphosis by feeding them with cultures of various
forms of diatom.

A complete account of the development of Asterias rubens by Dr.
Geniniill is now in the press, and will shortly be available to all
zoologists ; by Dr. Gemmill's kindness, however, we are allowed to
make use of some of his results which are as yet unpublished.
Field (1894) has given an account of the segmentation of the egg
and of the early larval stages in the development of the American
species (Asterias vulgar is). We have also an account of the full-grown
larva, and of the metamorphosis of Asterias pallida, by Dr. Goto (1897).
Now Asterias pallida is a mere synonym for Asterias vulgaris, and this
starfish is considered by systeinatists to be very closely allied to
Asterias rubens, the common British starfish, of which some indeed
consider it to be a local variety. By piecing together, therefore,
Field's, Gemmill's, and Goto's observations a fairly complete story
can be made out, and it is important to notice that in most important
points Goto's results demonstrate that, in so far as the building
up of the adult organs is concerned, Asterias pallida agrees very
closely with Asterina gibbosa. As the organogeny of the latter
species has been very thoroughly worked out we can thus use the

458 INVERTEBKATA CHAP.

data derived from it, with some confidence, in filling", in the gaps in
our story of asteroid development.

Before entering on this subject, however, there are certain
practical questions to be considered. Loeb, in his work Die chemische
Entwicklung des tierischen Eies (1910), states that the eggs of
Asterias are not ripe when laid, but ripen after lying in sea-water for
five or six hours. This seems to be a most misleading statement.
The eggs when shaken out of the excised ovary, or when made to
exude through the genital openings by the application of pressure,
are certainly unripe. They are surrounded by a glassy choriou
which disappears in a few hours and renders them fit to receive
the spermatozoa. But if perfectly ripe males and females be selected,
they will often emit their genital products spontaneously, and then
every egg which is emitted is capable of instant fertilization.

As to methods of preservation and of preparation a few words
may be said here. Goto used corrosive sublimate, with a certain pro-
portion of glycerine and of acetic acid, to preserve the larvae, but it is
exceedingly doubtful whether his histological results are at all reliable.
Further, this preserving fluid has one strong disadvantage, it is strongly
acid, and, as a developing Echinoderm contains numerous calcareous
deposits, the sudden solution of these is apt to generate quantities of
carbonic acid gas, which distend and tear the tissues. The cavities so
produced, which even so great an authority as Ludwig (1882) has
regarded as existing in the living animal, are nevertheless only
artefacts.

Faced with this difficulty, we ourselves, many years ago,
adopted a method of preservation which, although it has numerous
drawbacks, still yields better results with Echinoderm larvae than
any other. This method consists in adding a half per cent or even a
quarter per cent solution of osmium tetroxide to the watch-glass
containing the eggs and larvae, and leaving them in the mixture till
they are thoroughly impregnated with it and have assumed an
almost black colour. They are then transferred to a bottle containing
Mtiller's fluid (which is a mixture of the solutions of bichromate
of potash and sulphate of soda), in which they remain for twenty-four
hours at least, though several months' immersion in this fluid does not
hurt them. After treatment with Miiller's fluid they are rinsed
in distilled water, and then dehydrated by being passed successively
through various grades of alcohol. They are embedded in celloidin
and then in paraffin, according to the method described in Chapter II.
They may or may not be stained in borax-carmine before being
embedded, for the effect of this is merely to darken their colour and
render them more easy to orientate before finally making up the
blocks of paraffin. In all cases the sections are finally stained on
the slide in Grenadier's haeruatoxylin.

The penetration with osmium tetroxide gives a black stain of a
diffuse kind ; this is, in fact, due to a deposit of the metal osmium in the
cells, and it is difficult under these circumstances to get the ordinary

xvi ECHINODERMATA 459

staining agents to act on tissues so impregnated. It is found in
practice that if the sections be immersed in a strong solution of
borax-carmine for twenty-four hours they absorb little or no stain ; if,
however, after this treatment they are transferred to a dilute-solution
of Grenadier's haematoxylin in distilled water they will become
densely stained.

The advantages of this method are, (1) that the unsaturated chromic
acid in tlie bichromate of potash acts on calcareous deposits so slowly
and gently that they are dissolved without any accumulation of
carbonic acid gas resulting, and without any tearing of the surround-
ing tissues, because such carbonic acid as is produced is dissolved in
the water of the solution as fast as it is produced ; (2) that the form of
the cells and tissues is preserved with the most exquisite faithfulness,
such delicate structures as tine flagella being clearly visible when an
immersion lens is used.

If a section of a larva preserved in osmium tetroxide and Midler's
fluid be compared with a section of one preserved in corrosive sublimate
it will be seen that in the latter there is what one might almost term a
clotted appearance, i.e. the delicate cells of the connective tissue
tend to cohere in lumps, and the cytoplasm is seen, when subjected
to minute examination, to be somewhat shrunken, and to stain badly ;
whereas in the osmium tetroxide preparation the individual forms of
these connective tissue cells are exquisitely preserved, and their
cytoplasm is deeply stained and sharply distinguished from the
semi-fluid ground substance in which they are immersed.

The disadvantages of the method are, (1) that it renders the objects
so treated very brittle, and hence arises the absolute necessity of
embedding' in celloidin. For this reason it is less suitable for dealing
with yolky eggs, like those of Cribrella and Solaster, than with
comparative yolkless eggs, like those of Asterias, since the combina-
tion of the osmium tetroxide with the particles of yolk is extremely
hard and resisting to the knife ; (2) if applied to embryos of any size
the osmium tetroxide is apt to form a hard black crust on the
outside, and to prevent the penetration of the fixing fluid to the
interior of the specimen, which is thus badly preserved. For this
reason we have sometimes used a dilute solution of osmium tetroxide
(•25 per cent), and then allowed it to act for a considerable time,
because the fixative is thus enabled to penetrate to the interior.

For the preservation of the delicate pelagic larvae which occur
in the life-histories of the least modified Echinoderms no other
method gives results of equal value to this one. The difficulty
of brittleness can be got over by the use of the celloidin-paraffin
method of embedding, by good razors, and by restricting the period
of embedding in the hot paraffin as much as possible. For yolky
embryos and larvae, like those of Solaster, the mixture of corrosive
sublimate and acetic acid, in spite of its disadvantages, will probably
give the best results on the whole.

For making whole mounts other means must be adopted. Good

460 INVEETEBEATA CHAP.

results may be attained by the following method :— The larvae are
deluged with the strongest formalin (40 per cent solution) ; this is
neutralized before being used by having a piece of chalk immersed
in it. The formalin is only allowed to act for a couple of minutes,
and the larvae are at once transferred to absolute alcohol, to which
a drop of strong ammonia has been added. They are then stained
in a solution of either eosin or safranin in absolute alcohol, which
must be allowed to act for at least twenty-four hours, preferably
for several days. Then, drop by drop, at considerable intervals, oil
of cloves is added, — it is best to prolong the period of the addition
of oil of cloves over several days, — and then the larvae are transferred
to pure oil of cloves for several days. Finally, they are placed in
the well of a concave slide and a drop of a thick solution of Canada
balsam in xylol is placed upon them ; the oil of cloves flies off by
surface tension to the periphery, and can be — if the operation is
skilfully performed — almost entirely removed by blotting-paper. A
coverslip is now gradually pushed over the preparation from, the
side, so as to avoid the formation of bubbles, and in this way a
permanent preparation is made.

For younger stages, where there is not so much gelatinous tissue
as in the older larvae, a simpler method has been invented by Professor
Graham Kerr. He fixes them by immersing them (when freed from
as much of the salt water which clings to them as possible) in
absolute alcohol. They are stained in safranin dissolved in absolute
alcohol, and are then mounted in balsam dissolved in absolute alcohol.
Only a thin solution of this can be obtained, and it shrinks greatly
in the drying, but by patient addition of fresh solution, as that which
is just added dries, very beautiful permanent mounts may be obtained.

ASTERIAS

The egg of Asterias segments with great regularity into blasto-
meres of approximately equal size. It is a beautiful example of
indeterminate segmentation. The result of segmentation is a hollow
blastula, and it can be shown experimentally that, up to the 500-cell
stage, this blastula is not functionally specialized in any way, but
that any sufficiently large fragment cut from it will heal up by the
approximation of its edges, and so form a miniature blastula which
will develop into a perfect miniature larva. At about the 1000-cell
stage the cells develop cilia, and the blastula begins to rotate within
the egg-membrane, which it soon bursts, and it then rises to the
surface of the water and begins its existence as a free-swimming
larva. Certain of the Porifera and of the Coelenterata are the only
species of animals, outside the phylum Echiuodermata, in which the
larval existence is begun as early as it is in the development of
Asterias.

At the end of a day of free-swimming life the blastula begins to
be converted into a gastrula. The blastula loses its spherical shape

xvi ECHINODEKMATA 461

and becomes flattened on one side, which we shall term the posterior
side of the larva. In the middle of this flattened surface an invagina-
tion makes its appearance which is the beginning of the archenteron.
This invagination is of small diameter compared with the diameter
of the larva, and, in contradistinction to all the gastrulae so far
studied, a wide space, the primary body-cavity or blastocoele,
intervenes between endoderm and ectoderm. In most gastrulae a
slit-like blastocoele is present, but in Asterias it is enormous.

As the invagination progresses — or, according to Field, from
its very beginning — cells are budded off from the invaginating
surface into the blastocoele. These cells are termed mesenchyme.
The " wandering " of these cells seems to be effected by their emitting
long filamentous pseudopodia which span the blastocoele, and along
these strands the body of the cell glides like a drop of dew on a spider's
web. From the mesenchyme an exceedingly delicate gelatinous
connective tissue is formed, since the mesenchyme cells and their
pseudopodia secrete a few intercrossing fibres ; but the fluid " ground-
substance," which from the beginning has occupied the cavity of
this blastocoele, forms the great mass of the "tissue" until the
completion of metamorphosis.

As the invagination proceeds the gastrula grows in length,
changing its shape from a hemispherical to a cylindrical form, and
when the archenteron has attained about two-thirds the length of
the larva, it develops at its end a thin-walled vesicle, and the process
of gastrulation may be said to be complete. From this vesicle
mesenchyme cells continue to be budded off. The ectoderm cells at
the anterior pole of the larva become rather more columnar than
elsewhere (ap, Fig. 356, C), and bear longer cilia. This thickening
we may regard as a rudimentary sensory apical plate, but no nerve-
fibres have as yet been detected at the base of these cells.

In Asterias rubens, according to Gemmill, the formation of
mesenchyme does not begin so early as in Asterias vulgaris, no
mesenchyme at all being formed in the British species until invagina-
tion is well advanced.

From the vesicle at the apex of the archenteron two lateral
pockets grow out (Fig. 356, D). These are the rudiments of the
coelomic sacs, and they soon become completely cut off from the
archenteron, which in this way becomes divided into coelom and
gut. It is not clear, from the accounts which we possess, whether
the two coelomic sacs are, or are not, at first united across the middle
line by the remains of the original vesicle ; the coelomic sacs certainly
are united in this way in the larvae of Ophiuroidea and Echinoidea.
From the walls of the coelomic sacs more mesenchyme cells are
given off. The pseudopodia of these cells, which, as we have seen,
span the blastocoele, become in many cases muscular, and confer on
the larva powers of bending and of changing its shape.

The anus is nothing but the persistent opening of the blastopore,
but the mouth is the external opening of a wide funnel formed by an

462

INVEKTEBKATA

CHAP.

ectoderinic invagination situated at about one-third the length of the
larva from its front end. This invagination is of course the stomo-
daeum. Before the stomodaeum meets the gut, the latter becomes
divided by two constrictions into three regions. Of these regions the
hindermost is the intestine, the middle one becomes globular and
forms the stomach, whilst the most anterior forms the endodermal
portion of the oesophagus which meets and fuses with the stomodaeum

B

mes

coe

FIG. 356. — Stages in the early development of Asterias nilgaris. (After Field.)

A, blastula in optical longitudinal section. B, gastrula in optical longitudinal section showing the
formation of mesenchyme. C, older gastrula in optical longitudinal section. D, transverse section of
a larva slightly older than that represented in C, showing the formation of the coelom. ap, apical disc ;
coe, coelornic sac originating as pouches from the nrchenteron ; j/ies, mesenchyme ; rex, vesicle at the apex
of the archenteron.

(Fig. 357, B), and thus completes the larval oesophagus. Along
the sides of this oesophagus a V-shaped band of strongly ciliated
epithelium is differentiated, which is termed the adoral ciliated
band (Fig. 357, C). It seems to be formed from both the ectodermal
and the endodermal region of the oesophagus. The angle of
the V is situated behind in the mid-ventral line. The limbs of
the V pass up the sides of the oesophagus, and their terminations are

XVI

ECHINODEKMATA

463

connected by a much less strongly ciliated band, which passes round
the dorsal side of the oesophagus just behind the mouth.

It is commonly taken for granted that the function of the adoral
band is to direct a stream of water carrying minute organisms into
the mouth, and that it is in this way that the larva secures its
nourishment. Some years ago we made some observations on
the function of the homologous band in the larva of Echinus,
and it seems to us that the main function of the adoral ciliated
band, like the function of the cilia in the transverse grooves
running across the labial palps of Pelecypod Mollusca, is to remove
excess of food from the neighbourhood of the mouth. The minute
organisms, which constitute the bulk of the food, may be seen to be
carried in by a current which passes into the stomodaeum at its
dorsal border. This current seems to be caused by the cilia of the

ctilong

cillong

oes

FIG. 357.- — -Young larvae of A sierras vulgoris. (After Field.)

A, about three days old, from the side. B, about four days old, from the ventral surface. C, about
five days old, from the ventral side, a, anus ; cil.ad, adoral band of cilia ; cil.Jong, longitudinal ciliated
band ; int, intestine ; oea, oesophagus ; at, stomach ; stom, stomodaeum.

principal longitudinal band (v. infra], aided no doubt by the cilia
of the dorsal side of the stomodaeum. At the ventral end of the
stomodaeum particles may lie seen to be flung outwards violently-
hence it is apparent that the current produced by the adoral band
is directed outwards. The food accumulated in the outer end of
the stomodaeum is transferred to the stomach, not by the action of
cilia but by peristaltic muscular contractions.

Whilst these changes have been taking place other events have
been occurring. The cilia, which covered the whole surface of the
blastula and gastrula, become specially abundant and long over the
course of a sinuous band of thickened epithelium which is termed
the longitudinal ciliated band (cillowj, Fig. 357, A), and which is
the principal locomotor organ of the larva. Over the rest of the
surface they do not disappear, but become very sparse. This is due
to the passive stretching of the epithelial cells in these regions,
due to the increase in the pressure of the blastocoelic fluid.

The longitudinal ciliated band is also found in the larvae of

464 INVEKTEBRATA CHAP.

Ophiuroidea, Echinoidea, and Holothuroidea. It consists of two
sides, and of an anterior and of a posterior cross-bar. The anterior
cross-bar is situated in front of the mouth, and the posterior cross-
bar in front of the anus. Neither cross-bar is straight, both are
bent into the form of loops. The loop formed by the anterior cross-
bar is bent back along the ventral surface of the prae-oral region or
forehead of the larva, and it is termed the prae-oral loop, and the
area which it surrounds is termed the frontal field. The loop
formed by the posterior cross-bar bends forward along the ventral
surface in front of the anus, and the area which it surrounds is called
the anal field.

When the alimentary canal has been completed by the union of
the stomodaeum and oesophagus the larva is able to feed, and, if
suitable diatoms be provided, it will live and grow, even in a com-
paratively small aquarium, without any change of water. Dr.
Gemmill has reared the larvae of Asterias rubens for over two months
in his laboratory at Glasgow, until they had completed their meta-
morphoses ; and this feat has also been accomplished with the larvae
of Asterias glacialis by Professor Yves Delage in his laboratory at
Roscoff.

As the larva increases in size the tissue of the longitudinal ciliated
band grows more quickly than adjacent regions of the ectoderm, and
the band becomes thrown into folds. These folds form lobe-like out-
growths termed larval arms, which correspond in number, position,
and size on the two sides of the body, and confer on the larva a
" bipinnate " appearance, whence the name Bipinnaria. Mortensen
(1898) has invented a nomenclature for the larval arms of Asteroidea
and the homologous structures in other Echinoderm larvae, and we
shall follow his nomenclature in this book.

Before the larval arms have attained any size the prae-oral loop
becomes separated from the rest of the longitudinal ciliated band, and
this primary band becomes, in this way, divided into two secondary
bands, which we shall term the prae-oral and the post-oral bands
'respectively (pr.o.lj, p.o.b, Fig. 358).

In the Bipinnaria larva of Asterias vulgaris the prae-oral band
carries only two larval arms, which are termed the prae-oral arms
(pr.o.a, Figs. 358, 359), and the frontal field is somewhat quadrangular
in shape. But in the larvae of the European species, Asterias rubens
and A. glacialis, the prae-oral band develops in addition a median
anterior arm, directed forwards, termed the median ventral arm,
and the frontal field is consequently triangular in shape. From the
post-oral band, in all three species of Asterias, there is developed an
anteriorly directed arm, which is termed the median dorsal arm
(m.d.a, Fig. 358). From the sides of the post-oral band, about one-
third the length of the larva from its anterior end, there are given
off two arms, termed the antero-dorsal arms (a.d.a, Fig. 358). Still
farther back, at rather more than two-thirds the length of the larva
from its anterior end, two similar arms arise termed the postero-

XVI

ECHINODEKMATA

465

dorsal arms (p.d.a, Fig. 358). Where the sides of the post-oral
band pass into the anal loop two long arms are developed, termed
the postero-lateral arms (p.l.a, Fig. 358). Finally, from the sides of
the anal loop two short arms are developed, termed the post-oral
arms (p.o.a, Fig. 358).

The two coelomic sacs are, for a considerable time, two somewhat
rounded pockets lying at the sides of the oesophagus. The one on

B

rn.da.

pda

irit

FIG. 358. — Fully developed Bipiimaria larva of Asterias vulgar is, about three weeks old.

(After Field.)

A, from the ventral surface. B, from the dorsal surface, a, anus ; u.il.n, anterior dorsal arm ; i:il.ml.
adoral ciliated band ; fax, anterior fusion of right and left coelomic sac; int, intestine ; l.coe, left coelomic
sac ; iii.il.a, median dorsal arm ; «i.yi, madreporic pore ; uvs, oesophagus ; p.d.a, postero-dorsal arm ; p.l.u,
postero-lateral arm ; yi.o.a, post-oral arm ; ii.o.b, post-oral band of cilia ; pr.u.K, prae-cu-al arm ; pr.o.li,
prae-oral band of cilia ; r.coe, right coelomic sac ; st, stomach ; stem, stomodaeum.

the left side sends up a short vertical outgrowth which fuses with a
slight inward dip of the ectoderm, and in this way forms a canal
leading to the exterior. The opening of this canal is termed the
primary madreporic pore (m.p, Fig. 359), and the canal itself is
termed the pore-canal. Its wall is covered with cilia which beat
inwards and strive to distend the coelomic sac with sea-water.

Twenty years ago Field (1894) stated that, in the case of Asterias
vulgar-is, the right coelomic sac formed a similar pore-canal, terminat-
ing in a right madreporic pore (m1^1, Fig. 359), which soon, how-

r.coe

VOL. i

2 H

466

INVEKTEBKATA

CHAP.

'llong

stom

ever, became obliterated. No subsequent observer recorded the exist-
ence of this right madreporic pore, although the larvae of Asterias
were raised by thousands for experimental purposes by Driesch,
Herbst, and others ; but quite recently Dr. Gemmill has been able to
confirm Field's statement. He finds that a right madreporic pore is
formed in about one in every ten larvae of Asterias rubens, and in
one out of every two larvae of Asterias glacialis. In all cases it very
soon closes.

The ajipearance of a right and left madreporic pore is the first

indication of what is really the key
to the understanding of Echinoderm
development, viz. the fact that the two
sides of the larva originally gave rise
to precisely similar organs, but that
some of these organs grew and de-
velo'ped on the left side while they
atrophied on the right, and that
thus an asymmetry was produced.

The coeloniic sacs now begin
to grow in length until they form
long, narrow, cylindrical cavities,
reaching from the prae-oral region
of the larva to the posterior end ;
and by their form and relations
they merit the name "water-tube,"
bestowed on them by Agassiz
(1864). The right and left water-
tubes meet one another in the prae-
oral lobe and fuse into one (fus,
Fig. 358, B), but elsewhere they
remain separated from one another by
the alimentary canal, and above and
below this by a vertical mesentery.

Now a constriction appears
just behind the madreporic pore,
which almost, but not quite, divides
the left water-tube into anterior
and posterior portions. On the right side no such constriction is
formed until considerably later. The front division of the left water-
tube may be termed the left anterior coelom, whilst the hinder
division is named the left posterior coelom (l.p.c, Fig. 360, A).
The posterior portion of the left anterior coelom swells out slightly,
and begins to form five lobe -like outgrowths arranged in an open
curve. This swelling and its lobes are the rudiment of the water
vascular system, and are termed the hydrocoele (hy, Fig. 360). The
most dorsally situated lobe is numbered (1), the next (2), and so on.
Occasionally a similar five-lobed outgrowth, which we may term the
right hydrocoele, is formed as an outgrowth from the right water-

FIG. 359. — Larva of Asterias -culijaris
four days old, viewed from the dorsal
surface, .showing two madreporic pores.
(After Field.)

Names as in the preceding H^urr. In
addition, l.coe, left coelomic sac ; rn.ji (left),
persistent madreporic pore ; m'/il (right), tran-
sitory madreporic pore ; r.me, right coelomic
sac.

xvi ECHINODEIiMATA 467

tube. In this case this water-tube becomes completely divided into
anterior and posterior portions, which we may term right anterior
and right posterior coeloms respectively, just as the left is
normally. This formation of a second hydrocoele was first described
by us in Asterina (1896).

Somewhat later, near the mid-dorsal line but to the right of it, a
small sac is formed. According to Field (1894) it just appears as a
solid bud of cells in the blastocoele, but in Asterina gibbosa (Fig. 365)
it is certainly budded off from the posterior wall of the right side of
the anterior coelom, with which it remains connected for some time
by a solid string of cells. The bud is, from the first, nearly but not
quite solid ; it would be correctly described as a very thick-walled
evagination of the right anterior coelorn. It is soon cut off from the
anterior coelom, and then its cavity rapidly enlarges and it becomes
thin-walled.

In Asterias Goto (1897) has seen this cavity connected by a string
of cells with the left anterior coelom, but it is practically certain
that a re-examination of this point will show that Asterias and
Asterina agree in essentials. Gote's observations are exceedingly in-
complete, and it is iby no means clear that the " scattered string of
cells," which he saw connecting the sac with the left anterior coelom,
represents the original connection of the sac with the coelom.

This sac may be termed the madreporic vesicle. According to
Gemmill it executes slow pulsations. It may be compared to the
pericardial vesicle of Balanoglossus (see p. 575). We formerly
(1896) regarded the madreporic vesicle as the vestigial right hydro-
coele, but the observations of Gemmill, who has seen this vesicle and
a well-developed right hydrocoele present in the same larva, render
this view untenable.

METAMORPHOSIS OF ASTERIAS

With the formation of the madreporic vesicle, and of the rudiment
of the water vascular system, the Bipinnaria has reached the summit
of its development as a free-swimming organism. It now begins to
prepare to take up a fixed life, and with this change in habits the
metamorphosis may be said to begin. From the anterior end of the
larva, between the prae-oral and post-oral bands, there grow out three
clubbed arms which are not ciliated in the larva of A. vulgaris, but
in the larva of A. rubens and of A. glacialis the median ventral " arm "
of the prae-oral ciliated band is continued on to them. These arms
contain diverticula of the anterior coelom. One is median and dorsal
(br.med, Fig. 360), and the other two are situated symmetrically to
the right and left of it (br.lat, Fig. 362). These processes are termed
the brachiolar arms, and the larva is now termed a Brachiolaria.
It still swims, but it occasionally attaches itself to the side of the
vessel in which it is contained by the brachiolar arms, which appar-
ently act as suckers. Goto states that the cells forming the walls of

468

INVERTEBEATA

CHAP.

the coelomic vesicles develop muscular fibrils at their bases, which
are for the most part disposed circularly, but some' of which pursue a
longitudinal course. Now the brachiolarian arms differ from the
other larval arms in possessing hollow outgrowths from the coelom
within them, and it appears certain that the longitudinal muscular
fibres accompanying these outgrowths can cause a retraction of the
central portions of the tips of the brachiolarian arms, and thus enable
them to act as suckers.

As we have noted above, the right and left coelomic sacs fuse with
one another in the prae-oral lobe, and the left becomes almost divided

mda

ada

FIG. 360. — Lateral views of an advanced Bipinnavia of Asterias vulgaris, in which the
brachiolarian arms are just appearing. (After Goto.)

A, outline view to .show the segmentation of the coelom. B, more detailed skrtch. Letters as in
Fig. 358. In addition, a.c, anterior coelom ; lir.a, rudiment of anterior median brachiolarian arm ; l<j,
hydrocoele ; 1-5, the five lobes of the hydrocoele ; l.p.c, left posterior coelom.

into two by a constriction which appears just behind the hydrocoele.
Somewhat later a similar constriction appears in the right coelomic
sac, and by these two constrictions two posterior regions, the left
posterior coelom and the right posterior coelom, become marked
off from the left and right coelomic sacs. The left posterior coelom
begins to extend beneath the gut over to the right side ; this extension
is known as the right ventral horn of the left posterior coelom, and
its formation causes the whole sac to take on the form of a U (Fig.
361). It fuses with the right coelomic sac in front of the constric-
tion, separating it into anterior and posterior portions — in a word, it
fuses with the right anterior coelom. Soon, left and right anterior
coelomic sacs, already fused in front, become completely merged in
one another so as to form a single anterior coelom. The right

XVI

ECHINODERMATA

469

posterior coelom becomes entirely cut off from the anterior coelom :
it is termed the epigastric coelom by Goto, who thought that it
was formed by the growth of an independent longitudinal septum,
but this error has been corrected by Gemmill.

By the time that these changes have been accomplished the
brachiolar arms have been formed ; and in the centre of the circle
formed by them a circular disc of thickened glandular ectoderm
appears. This is the organ for permanent fixation (fix, Fig. 362).
Holding on by its brachiolar arms the larva brings this disc into
close contact with the substratum and thus permanently fixes itself.

The larva may now be said to be
differentiated into a posterior region
containing the stomach, the intestine,
the hydrocoele, and the right and left
posterior coelorns ; and into an anterior
region, consisting of the prae-oral lobe,
containing the mouth, oesophagus, and
the anterior coelom. The anterior region
may be termed the stalk, the more
posterior the disc. Once the larva has
become firmly attached the stalk is pro-
gressively shortened (Fig. 362, B).

The stone-canal makes its appear-
ance as an open groove of ciliated
epithelium, situated on the anterior
aspect of the septum dividing anterior FKJ. 361.— Ventral view of a

from left posterior COelomS. It begins Bipinnaria of Asterias mdgaris

just beneath the inner end of the pore-
canal, and it runs down to the spot
where the anterior coelom is "beginning

tO be pinched from the hydrOCOele. Letters as in preceding figure.

On the posterior aspect of the septum r" ;adfftion; ?!^lcl- r!ght ventral ho;'!

£ of left posterior coelom; r.p.c, right-

there appears a groove-like outgrowth ot posterior coeiom.

the left posterior coelom. This groove

is the rudiment of the peri-oral coelom. It grows into a tube which
extends in the form of a slight crescent beneath a faint bulge of the
stomach, which is the rudiment of the adult stomach.

The stomodaeum becomes disconnected from the endodermal
portion of the oesophagus : it persists for a brief time as a shallow
pit of the ectoderm, but eventually disappears entirely, and the
oesophagus becomes, as metamorphosis proceeds, a less and less
conspicuous appendage of the stomach. The anus of the larva is
also obliterated, and the intestine becomes shortened till it forms a
very short tag attached to the stomach. According to Gemmill this
tag persists throughout metamorphosis, and from it the rectum of
the adult is developed.

Five thickened lobes now appear on the ectoderm covering the
right posterior coelom. These are the first traces of the arms of the

st

of the same age as that shown
in Fig. 360, in order to show
the mutual relations of the
coelomic cavities. (After Goto.)

470

INVEKTEBKATA

CHAP.

future star-fish and are termed collectively the aboral disc. As
the ventral horn of the left posterior coelom extends further and

FIG. 362. — Lateral views of the brachio-
larian phase of the larva of Aster 'i as
vulgaris in various stages of fixation
and metamorphosis. (After Goto.)

A, earliest stage : temporary fixation by
means of the brachiolarian arms: prae-mal
lobe undiminished. B, later stage: permanent
iixation by means of the fixing disc: the
prae-oral lobe is much shrunk. C, still later
stage : the prae-oral lobe has almost dis-
appeared : metamorphosis almost complete.
Lettering as in Fig. 300. In addition,
fix, the disc by which the larva tixes itself;
rnnian numerals I-V, the rudiments of
the live arms.

brl

further round to the right, and grows in size, the right posterior
coelom and the disc covering it become displaced backwards, and

xvi ECHINODEKMATA 471

eventually come to occupy a position at the posterior pole of the
larva. At the same time other changes are occurring. The hydro-
coele becomes more and more grooved off from the anterior coelom.
The stone-canal is changed from a groove into a tube by the meeting
of its edges. As the hydrocoele becomes grooved off it exhibits a
dorsal horn and a ventral horn, and a central piece where it remains
for a time in connection with the anterior coelom. The ventral
horn extends round underneath the larva to the right side, in fact it
grows parallel with the left posterior coelom.

Thus the metamorphosis of the larva may be roughly summed up
as consisting in the preponderant growth of the organs of the left
side as compared with their antimeres on the right side (right hydro-
coele and right posterior coelom), together with the gradual atrophy
of the prae-oral portion of the larva which forms the stalk. The
lobes of the hydrocoele are the rudiments of the radial water-vascular
canals of the adult star-fish, and the completed arm consists of the
process o'f the aboral disc, into which an outgrowth from the left
posterior coelom extends, and to which the process of the hydrocoele
becomes applied. There is little doubt that the process of the aboral
disc, with its contained coelom, is to be regarded as an outgrowth of
the body, secondarily developed, in order to give support to that long
hydrocoele lobe, or radial canal, which was originally a free tentacle.
Each primary lobe of the hydrocoele develops lateral lobes in pairs, as
branches; of these two pairs are formed before metamorphosis is
complete. These are the rudiments of the paired tube feet.

The adult stomach appears, we have seen, as an outgrowth from
the larval stomach on the left side, in the region where the peri-oral
coelom has made its appearance as an outgrowth from the left
posterior coelom. As the new stomach grows out the peri-oral coelom
extends round it ; whilst outside it the left posterior coelom, whose
dorsal and ventral horns meet and fuse with one another, forms an
outer ring. At the same time short pouches grow out from the larval
stomach into the developing arms. These pouches are the rudiments
of the pyloric caeca of the adult, and the larval stomach becomes
the pyloric sac, whilst the adult stomach is really the eversible
sac which the star-fish wraps round its prey. The adult mouth is
formed by the fusion of the adult stomach with the ectoderm.

Only when the metamorphosis is nearly complete does the
rectum make its appearance. It grows out in the mesentery
separating the right posterior coelom from the left posterior coelom,
in the same mesentery, that is to say, in which the larval intestine
was situated, and, as mentioned above, Gemmill has shown that it is
formed from the stump of the larval intestine. The adult anus
appears later still ; it is eventually perforated in the right dorsal
inter-radius, using the word " right " in reference to the sagittal
plane of the larva.

The shrinkage of the prae-oral lobe is largely due to the change in
form of the ectoderm cells covering it — they change from a flat to a

472 INVERTEBEATA CHAP.

columnar form. The ectoderm covering the brachiolar arms is
involuted into pockets, and these involuted portions are attacked
and devoured by phagocytes. In Asterina all the ectoderm of the
prae-oral lobe is disposed of in this way ; but in Asterias, as the
prae-oral lobe shrinks in size, a good deal of the ectoderm which
originally covered it is drawn into the covering of the oral disc of
the star-fish. As the shrinkage of the prae-oral lobe goes on, the
sinuosities of the ciliated band, the " arms " of the larva, become
straightened out and thus obliterated. Finally, all that is left of
the prae-oral lobe is a small button projecting from the oral surface
of the star-fish (Fig. 362, C), but when the star-fish begins its free
life, as it wrenches itself free, the neck of this button is pulled out
into a long filamentous stalk .which eventually breaks through and
sets the star-fish free.

DEVELOPMENT OF OTHER ASTEROIDEA

We may now glance at the peculiarities of the larvae of other
Asteroids whose life-history has been studied. Quite a number of
" species " of Bipinnaria are known, but few of them can be assigned
to any definite species of Asteroid. The complete life-cycle is only
known in the case of Asterias rubens, A. glacialis, and A. vulgaris.

It has been doubted whether all Bipinnaria larvae develop
brachiolar arms, i.e. pass through a fixed stage. Gemmill has
recently shown that the larva of Povania pulvillus has such a stage ;
but extraordinary statements are made about the large Bipinuariae be-
longing to Asteroids of the family Astropectinidae, in which brachiolar
arms have never been observed. M. and C. Delap (1905) state that
in these larvae the star-fish rudiment is amputated from the posterior
half of the larva, the front half of which goes on living for a long
time after. Here is a matter which urgently requires reinvestigation.

We may now turn to the consideration of the development of
Asterina gibbosa, which has been worked out by us in considerable
detail (MacBride, 1896). This development has already been alluded
to more than once. Its main peculiarities concern («) the formation
of the larval gut and of the coelom, and (ft) the external appearance
of the larva.

With regard to (a) the first point, we find that Asterina gibbosa
has a prolonged embryonic life and only escapes from the egg-mem-
brane on the fourth day, when not only coelom, but also stomodaeum
and madreporic pore have been formed. The archenteron is spacious
and nearly fills the blastocoele. The coelom arises as an enormous
unpaired vesicle, constituting more than half the archenteron, and from
this vesicle prolongations, " tongues," extend backwards at the sides
of the gut (Fig. 363, B). Then transverse septa appear, which divide
off right and left posterior coeloms from an anterior unpaired coelom.
These septa are found in the " tongues" of the coelom, so that there
is an anterior portion of each tongue which belongs to the anterior

xvi ECHINODERMATA 473

coelom. The larval intestine is straight, and both it and the larval
anus disappear shortly after the animal enters on its larval existence ;
that is on the fifth day. The coelom is only separated from the gut
after the stomodaeum has broken through.

As for the second point (6), the larva has the form of a boot. The
sole of the boot is the prae-oral lobe, which is enormous, and the
" upper " of the boot is the body. The back of the boot corresponds
to the ventral surface of the larva, and here the larval mouth is
situated ; while the front of the boot is the dorsal surface. The
prae-oral lobe is surrounded by a thickened ridge which bears
specially long cilia, by the aid of which, and of the cilia of lesser
length which cover the ectoderm everywhere, the larva glides about
on the bottom. It uses the prae-oral lobe as a sucker, attaching the
thickened rim to the substratum on which it is moving, and then
retracting the centre. In the centre there appears, on the seventh day,

A B

coe

FIG. 363. — Frontal longitudinal sections of two early embryos of Asterina gibbosa,
in order to show the development of the coelom. (Original.)

A, stage in which the coelom is a spherical vesicle. B, stage in which the coelom is growing liack
in tongues at the sides of the gut. <tl, rudiment of gut : Wj>, blastopore ; coe, rudiment of the coelom.

a circular area of thickened glandular epithelium (Fig. 364). This is
the fixing disc, and by means of the secretion produced by it the larva
effects a permanent fixation to the bottom. Once this has been
accomplished the rim is destroyed by the same process as that by
which the brachiolar arms are removed in the Bipinnaria larva. The
whole prae-oral lobe shrinks, until final atrophy takes place and the
larva wrenches itself free and walks away as a little star-fish.

The internal changes which take place during the larval life, and
the metamorphoses, are known in detail. Let us go back to the time
when the transverse septa are found in the coelom. The septum is
formed on the left side before it is formed on the right, and in both
cases it begins at the dorsal side and grows down to the ventral
surface. On the left side, the septum, after formation, becomes
perforated by two holes, a dorsal and a ventral one. In this way a free
passage of fluid between anterior and posterior coeloms is allowed ;
and as the cells of the coelomic wall, as in the Bipinnaria larva,
secrete muscular fibrils, and the larva can change its shape very much,

474

INVERTEBRATA

CHAP.

this is very necessary. Similar holes are formed in the transverse
septa in the Bipinnaria larva, as we have already seen.

The hydrocoele arises as a bulge on the left side of the posterior
part of the anterior coelom, whilst the madreporic vesicle is formed
as a bud from the posterior end of the anterior coelom, a little to
the right of the median line. It becomes hollowed out, and is for a
time attached to the wall of the anterior coelom by a string of cells,
but this is soon broken and the vesicle detached. A right hydrocoele
with five well-developed lobes, or sometimes with only three or only one
lobe, is sometimes developed, and often in this case the madreporic
vesicle is suppressed, which is the reason why we formerly regarded
the two structures as homologous. Even before metamorphosis
begins the left posterior coelom is wider than the right, and begins to
send out a ventral horn which underlies the right coelom, and the
peri-oral coelom originates as a pocket of the left posterior coelom.

FIG. 364. — Views of a free-swimming larva of AstcriiKi ijililmm five or six days old.

(After Ludwig.)
A, from in front. B, from the side and above, ji.r, lixing disc. prJ, prae-oral lobe.

In Asterina gibbosa, as soon as metamorphosis commences the
stone-canal makes its appearance as an open groove on the anterior
face of the transverse septum, as in Asterias. This groove becomes
closed in the middle, but opens at one end into the hydrocoele, and at
the other end into the anterior coelom just below the opening of the
pore-canal. Then five outgrowths of the coelom shaped like inverted
wedges are formed. Of these outgrowths, one arises from the anterior
coelom and four from the left posterior coelom (p.h, Fig. 366). They
project against the ectoderm and alternate with the five lobes
of the hydrocoele. These outgrowths are soon cut off from the
coelom, and lie between ectoderm and coelomic wall as flattened
vesicles. They are the rudiments of the perihaemal system of
spaces.

The arms grow out as blunt outgrowths from the region of the
body occupied by the left posterior coelom, and into each of them an

XVI

ECHINODEKMATA

475

outgrowth from this coelom extends. It is noteworthy that, counting
the arms from before backward, No. 1 arm is really situated over
No. 2 lobe of the hydrocoele, and eventually fuses with it ; and later
in the metamorphosis, when the ring-shaped growth of the left
hydrocoele and the left posterior coelorn is complete, No. 1 hydro-
coele lobe comes to lie under No. 5 arm. The neighbouring angles
of adjacent perihaernal spaces grow into the arms beneath the
hydrocoele lobe, and in this way the two radial perihaemal canals,
which are found in each adult arm, are formed. The external peri-
haemal ring-canal is formed by the fusion of the main portions of
these spaces.

The internal perihaemal canal is formed by a circular extension
of the hinder part of the anterior coelom which is included within the

st

Ip.c P

FIG. 365. — Longitudinal frontal sections of larvae of Asterittti tjibbosa, to show the segmenta-
tion of the coelom and the origin of the hydrocoele and madreporic vesicles. (Original.)

A, section of larva aliout live days old. B, section of larva about six days old. C, section of larva
about six and a half to seven days old. <ie, anterior coelom ; a.st, rudiment of adult stumach ; li,y, rudi-
ment of the hydrocoele ; 1, 2, etc., its lobes ; l.p.c, left posterior coelom ; HI. r, madreporic vesicle ; p.n.c,
rudiment of peri-oral coelom. r.p.e, right posterior coelom ; at, larval stomach.

body of the star-fish when the stalk finally disappears. This portion
of the anterior coelom, into which pore-canal and stone-canal open, is
known as the axial sinus (Fig. 366, dicv). The septum, which divides
it from the general body-cavity surrounding the stomach in the adult
star-fish, is nothing but the old transverse septum which separated the
anterior coelom from the left posterior coelom in the larva; and it
follows, therefore, that the general body-cavity of the adult is only
the ring-shaped left posterior coelom, which, with Goto, we may term
the hype-gastric coelom. The right posterior coelom of the larva
becomes the epigastric coelom of the adult.

In Asterias, Goto maintains that the perihaemal spaces appear as
solid masses of mesenchyme, lying on the ventral surfaces of the arms
when metamorphosis is complete, and that these spaces subsequently

476

INVERTEBEATA

CHAP.

become hollowed out ; but Gemmill has shown that this is an error
and that these spaces originate in Asterias in the same manner as
they arise in Asterina.

As metamorphosis proceeds the prae-oral lobe shrinks more and
more, and the neck of the lobe becomes constricted. The effect of

FIQ. 366. — Longitudinal frontal sections of larvae of Asterina gibbosa seven to eight days

old, to show the beginning of the metamorphosis. (Original.)

A, section through a larva in the dorsal region of the body. B, section through a larva near Hie
median region of the body. C, section through a larva in the ventral region of the body. Letters as
in previous ligure. In addition, p.h, rudiments of perihaemal spaces; p.h.1.2, rudiment of perihaemal
space intervening between lubes 1 and 2 of the hydrocoele ; ]>.h.-2.3, rudiment of perihaemal space
between lobes 2 and 3 of the hydrocoele, and so on ; sf.c, stone-canal (still an open groove).

this is to bring arm No. 5 closer and closer to hydrocoele lobe
No. 1 (Fig. 368). At the same time each hydrocoele lobe gives rise
to two pairs of lateral branches springing from its base. These are
the rudiments of the paired tube feet (Fig. 368, t.f), while the tip of
the primary lobe forms the azygous tube foot in which the radial canal
terminates.

xvi ECHINODEEMATA 477

The larval oesophagus or stomodaeum, as iu Asterias, becomes
disconnected from the larval stomach, shallows out and disappears.
The larval stomach, which, as we have seen, forms the adult pyloric
sac, hegins to give off blunt outgrowths into the cavities of the
nascent arms : these are the rudiments of the pyloric caeca
(Fig. 369). The adult stomach, begun as we have noted as an out-
growth on the left side of the larval stomach, increases in size and
comes in contact with the ectoderm at a spot between the dorsal and
ventral horns of the left posterior coelom. These horns meet above
it, and so the left posterior coelom is converted into a ring. Within
this ring lies the ring formed by the hydrocoele, and beneath this the
ring formed by the peri-oral coelom. The holes in the septum
dividing the anterior coelom from the left posterior coelom become
healed up, and with the progressive constriction of the neck of the

II

FIG. 367. — Views from the side of a larva of Asta-ina gilihusa seven clays old in the initial
stages of metamorphosis. .'After Ludwig.)

A, from the right side. B, from the left side. 1-5, lobes of hydrocoele. I-V, rudiments of arms ;

in-.l, juae-oral lobe.

prae-oral lobe the anterior coelom becomes divided into a transitory
portion, situated in the stalk, and a permanent portion, the axial
sinus, which is included within the disc of the star-fish. The hydro-
coele communicates with the anterior coelom not only through the
stone-canal, which has become a closed tube, but through an opening
in the neighbourhood of its third lobe which does not become closed
until metamorphoses is nearly complete.

The adult nervous system of Asterina arises as a plexus of
ganglion cells and fibres, beneath the ectoderm which overlies the
perihaeuial spaces and the lobes of the hydrocoele. Goto states
that, in Asterias, part of this ectoderm is derived from the longi-
tudinal ciliated band of the larva. If this statement could be confirmed
it would be a matter of great interest.

Of the development of the adult calcareous skeleton of Asterina
we have a full account from Ludwig (1882), and we have also some
information about the origin of the calcareous skeleton in Asterias
rubens from Bury (1895). The first traces of calcareous plates in

478

INVEKTEBKATA

CHAP.

Asterina, and in all other Echinoderms which have been studied,
are little triradiate spicules embedded in and produced by the
mesenchyme cells intervening between coelomic wall and ectoderm ;
each arm of the spicule, as it grows, bifurcates, and the forks of

adjacent arms join one

A B another, and in this way a

mesh is formed. From the
junction of the two forks
another arm is given off,
and, by a repetition of the
processes of forking and of
union of forks, a network of
calcareous meshes is slowly
built up.

The first spicules to
appear in Asterias and
Asterina are the rudiments

Asterina gibbosa eight days old, to show the of the terminal platCS (T,

T • T T • \ ^ ^

IE

FIG. 368. — Views from the side of a larva of

Fig. 370), which overarch and

progress of metamorphosis. (After Ludwig.)

A, from the right side. B, from the left side. Letters protect the azygOUS tentacles
as in previous figure. In addition, t.f, rudiments of i • i j-i • it,

paired tube feet. m whlch the P^aiy lobes

of the hydrocoele, or radial

water- vascular canals, terminate. Alternating with these terminal
plates arise five basal plates
(B, Fig. 370), one of which
surrounds the madreporic pore
and is the rudiment of the
madreporite of the adult^.
In the centre of the circle ol
basals there arises the so-called
dorso-central plate (D.C, Fig.
370). This plate does not lie
over the right posterior coelom
but rather to one side of it,
and the adult anus, which
appears at one side of the
dorso-central plate, is conse-
quently situated over the
mesentery separating the left
posterior and right posterior FlG 369-_Longitudin!ll frontal section tlirough

a larva of Asterina gibbosa about the same
age as those shown in previous figure.
(Original.)

coeloms.

The rectum, which is
formed as an outgrowth from
the larval stomach, lies in this
mesentery. On the ventral
side of the disc there appeal-
pairs of spicules alternating with the rudiments of tube feet. These
spicules are the rudiments of the ambulacral plates. The muscles

Letters as in Figs. 365 and 300. Tn addition, ale1,
rudiment of axial sinus ; py.r, rudiment of pyloric
caecum.

XVI

ECHINODEBMATA

479

connecting these plates with one another, by means of which the
arm can be bent and the ambulacra! groove closed, are derived
from the cells forming the walls of the perihaemal canals.

As metamorphosis approaches completion, the septum dividing
the peri-oral coelom from the encircling left posterior coelom is largely
absorbed, and the two cavities coalesce ; as remnants of this septum
there remain ten bauds, two in each arm, which constitute the
retractor muscles of the adult stomach. The adult mouth is formed
by the fusion of the wall of this stomach with the ectoderm ; there
is no adult stomodaeum. When the stalk has been almost absorbed
the little star-fish wrenches itself loose from the substratum by pulling
with its tube feet, and it walks away.

•%-& ^*'1

V ^i^O-^T

'^<<r *•

.

! -

! i : "• • ><r

T~- "r~-ip^'-;'^

w^-^" Jl^

DC F^

r* r* *^^ jf i ^» '

D.C. yVy/

FK;. 370. — Dorsal (i.e. aboral) views of two young specimens of Asterina gibbosa shortly
after the metamorphosis. (After Ludwig. )

A, yountj; stav-lish ten clays old. 15, younjj star-fish sixteen days old. n, adult anus ; n-.t, azygous
tentacle of water-vascular system ; B, basal plate; D.C, dorso-central plate; £, radial plate; '/', terminal
plate. In the specimen shown in figure B, only four basals are developed.

The post-larval development has been followed in Asterina.
The main points which have been determined concern the further
development of the skeleton and the development of the genital
system. We shall deal with the development of the skeleton first.
As the arms grow in length new tube feet are added in pairs, the
first formed tube feet remaining at the base of the arm, and,
alternating with the new tube feet, new ambulacral ossicles are
added. At the same time the terminal plates are carried out to the
tips of the arms, and new plates are intercalated between them
and the central plate. The most important of these, and the first
to appear, are the radials situated at the bases of the arms. The
names basals, dorso-central, and radials, it may be remarked, have
been bestowed on these plates from a suggested homology with the

480

INVEETEBEATA

CHAP.

plates which make up the skeleton of a Crinoid, the value of which
will be examined when we consider the development of a Crinoid.

The origin of the genital organs is very peculiar. About the
time that the metamorphosis is completed a peculiar fold appears
in the wall of the axial sinus which abuts against the left posterior,

w.ur

\

©

'n.r

FIG. 371. — Three figures to illustrate the development of the genital stolon, genital rachis,
and gonad in Asterina, gibbosa. (Original.)

A, vertical section of the disc of a specimen that lias just metamorphosed. Disc about '75 mm. in
'liameter. 13, horizontal section through one of the inter-radial septa of a specimen about 1'2 mm. across
the disc. C, Section through the incipient gonad of a specimen about 6 mm. across the disc, ab.s,
aboral sinus ; aU-i, axial sinus; i/.u, dorsal organ; r/en.r, genital rachis; gen.st, genital stolon; ;/"»,
gonad; gon.s, gonadial sinus; jn.i1, madreporic vesicle; ph, perihaetnal space; pr.g.in-v, primitive
germinal-involution ; st.c, stone-canal.

or, as we may now term it, the hypogastric coelom. This fold is the
rudiment of the strand called axial organ, dorsal organ, or genital
stolon, and formerly regarded as a heart (d.o, Fig. 371, A). At the
dorsal edge of the hypogastric coelom, where the remains of the
mesentery which separated it from the epigastric coelom are still to
be seen, an involution of the coelomic epithelium takes place which

xvi ECHINODEEMATA 481

projects into this fold. The involution, at first hollow, soon becomes
solid and is termed the primary germinal involution (p.y.inv, Fig.
371, A). The solid bud thus produced proliferates downwards into the
axial organ and forms the peculiar cells characteristic of this structure,
but it also proliferates laterally, to the right and to the left, and
forms a cord of primitive germ cells known as the genital rachis
(g.r, Fig. 371, B), which grows as a freely projecting rod right round
the disc of the star-fish until the two ends meet and a complete
circle is formed. The rod is, of course, covered with a thin layer of
peritoneum which is reflected over it ; it is supported in a sling of
peritoneum which grows out parallel with the rod and underneath
it, as a flap, which fuses with the body wall on both sides and
encloses a space called the aboral sinus (ah.s, Fig. 371, B).

At each side of the base of each arm a branch is given off from
the rachis enclosed in a branch of the aboral sinus. This branch
extends downwards and then along the arm, where it enlarges and
forms a bunch of diverging branches which constitute the genital
organ. Round each branch, of course, is a branch of the aboral
sinus, but this branch becomes cut off from the main part of the
sinus by the ingrowth of a septum (gon, Fig. 371, C). The genital
duct is formed as a solid outgrowth from the base of the genital
organ, where it joins the rachis. This outgrowth fuses with the
ectoderm and then becomes hollowed out. The process by which
a genital gland discharges itself bears a considerable resemblance to
the way in which an abscess finds its way to the surface.

Both Solaster and Cribrella agree, as far as the general form of
their larvae is concerned, with Asterina, though differing in details of
shape and size of the prae-oral lobe, and they have a quite similar
metamorphosis. But they differ in one most important respect,
they never develop a larval mouth, and the larval gut remains in
a most rudimentary condition, being merely a collar of more
columnar cells round the middle portion of the archenteron. The
hinder portion of the archenterou gives rise to the left posterior
coelom, whilst the front portion gives rise, not only to the single
anterior coelom, but also to the right posterior coelorn. From the
anterior coelom are also given off the hydrocoele and the nmdreporic
vesicle.

The credit of elucidating this extraordinary form of development
belongs to Masterman (1902), whose observations on Cribrella have
been confirmed in almost every point by those of Gernmill on
Solaster (1912). Masterman (1902), viewing this development as
primitive, regards the right posterior coelom as the antimere of the
left hydrocoele, and the left posterior coelom as a median structure
containing right and left elements. He terms the madreporic vesicle
the central coelom. i According to Gemmill, in Solaster the madre-
poric vesicle arises to the right of the middle line, as in Asterina.

There are obvious objections to regarding the shortened develop-
ment of an Asteroid, with a yolky egg, as capable of throwing light

VOL. I 2 I

482

INVEIITEBRATA

ciiAr.

on the primitive condition of the development of Asteroidea.
Gemmill's researches (1912) on Solaster allow of another interpreta-
tion of the type of development. In Solaster the posterior coelom
is not symmetrical, l.wt inclined to the left, and the area which
eventually forms the gut does not extend evenly all round the
archenteron. We might therefore derive the condition of affairs in
the larva of Solaster from the condition of things in the larva of

Asterina, by imagining that the
preponderant growth of the organs
of the left side has been pushed
so far back into the embryonic
period, that the gut-rudiment is

ac

swung out of the longitudinal

into a transverse position, and so
the open end, from which the
coelom is cut off, is directed to the
left instead of anteriorly.

Solaster is further remarkable
for the fact that, although it is
a star-fish with many rays, the
left hydrocoele has at first only
five lobes which all develop simul-
taneously, and additional lobes
are developed much later ; so that
in one and the same specimen,
when the more dorsal lobes of the
hydrocoele have already developed
lateral tube feet, and the peri-
haemal spaces in connection
therewith have been completely
FIG. 372.— Longitudinal frontal section of separated from the coelom, the

the larva of Solaster endeca.
Gennnill.)

(After

Inj, hyc.lrocoele ; /./<.'•, left posterior coelom;
r.ji.i; right posterior coelom.

more ventral lobes will still be
quite undivided, and the ad-

a.c, anterior coelom ; nl, alimentary canal ; jacent perihaeuial SpaCCS will

have the form of shallow evagina-
tions of the coelom. This circum-
stance seems to indicate that the number five, so characteristic of
the rays in all Echinoderrnata, was characteristic also of the ancestral
Echinoderm, and that where many rays are found this is not a
survival of a primitive state of affairs, but is a secondary
modification.

EXPERIMENTAL EMBRYOLOGY OF ASTEROIDEA

A great many experiments have been performed on the eggs of
Asteroidea, but in the case of many of these quite the same results
have been obtained with the eggs of Echinoidea, which have been
classic subjects of experimentation since the study of Experimental
Zoology started. So far as space will allow they will be mentioned

xvi ECHINODERMATA 483

when dealing with the Echinoidea, but there are some which are,
so to speak, peculiar to the Asteroidea.

It has been already mentioned that the fully developed gastrula of
Asterias is a long, sausage-shaped structure, and that the archeuteron
only reaches half-way through it (Fig. 356). Driesch (1895) made a
thick culture of these gastrulae, accumulating hundreds in a very
small quantity of water, and snipped at random in this water witli
a fine pair of scissors about 200 times. In this way he succeeded
in cutting a number of the gastrulae in pieces. Sometimes he found
that they were cut longitudinally and sometimes transversely. In
both cases, if the fragment included both endoderni and ectoderm, it
healed up by the approximation of its edges and formed a miniature
gastrula, which then developed further into a small but perfect
Bipiimaria. If, however, the gastrula was transversely bisected after
the thin-walled vesicle at the apex of the archenteron had made its
appearance, so that this vesicle was removed, then the truncated larva
healed up and went on developing, but it never formed a new
coelomic vesicle, although it takes on externally the form of a
Bipinnaria. The appearance of this vesicle, therefore, according to
Driesch, " negatively determines," i.e. limits the potency, that is, the
power of development possessed by the archenteric wall. Before
that vesicle appears a small fragment of this wall will grow and
rearrange its cells so as to form the three segments of the asteroid gut,
viz. oesophagus, stomach, and intestine, and in addition the terminal
vesicle ; but, when this has been once formed, then, even a larger
fragment of the archenteron is incapable of moulding itself into
more than oesophagus, stomach, and intestine.

Driesch regards this limitation of power as due to a progressive
" stiffening " of the protoplasm, which renders it less and less amen-
able to the regulating influence of the " entelechy," or indwelling
power, which, according to the vitalistic principle held by Driesch,
knows and wills what it wants to do with the material at its disposal.
A more humble explanation, and one more in accord with what we
know of other eggs, is that there exists a definite coelom-forming
substance which is at first diffused through all the cells of the gut
wall, but which becomes, as development proceeds, definitely localized
in one spot ; and if that portion of the gut be removed, the remainder
has no material which will allow of the development of the coelom.

Herbst (1896) showed that if a solution of 3'7 per cent of sulpho-
cyanide of potassium be made, and then three parts of this solution
be added to 100 parts of sea- water, the eggs of Asterias will develop
in this medium and will live on for four weeks, but that they do
not get beyond the blastula stage. The beginning of an archenteron
may be formed, but it degenerates into a granular mass of cells and
is absorbed.

These persistent blastulae, though possessing the clear trans-
parence which indicates health, differ from the normal blastulae in
possessing abundance of inesenchyme in the interior. The normal

484 INVERTEBRATA CHAP.

blastula of Asterias does not develop mesenchyme cells, these are
only formed ai'ter the gastrula stage has been reached. In these
abnormal blastulae the rneseuchyme cells are given off from the
vegetative pole, while from this same pole mesenchyme is given off
in the normal blastula of Echinus before an archenteron has been
formed.

Herbst concludes that the action of the sulphocyauide has
changed the development of the blastula from the Asteroid to the
Echinoid type. This may be admitted, but the question arises how
this comes about. The vegetative pole of the egg is the region which,
in the Asteroid, is invaginated to form the archenteron, and from
the apex of the archenterou the mesenchyme is given off; so that
the mesenchyme originates from the same region in the normal and
in the abnormal larva. Further, there is often, as we have seen in
the abnormal larva, an attempt to form an archenteron which is,
however, abortive.

We may draw the conclusion, therefore, that the normal develop-
ment consists of distinct processes which are to a large extent
independent of one another. On these processes the drug acts in a
selective way ; it inhibits the process of forming an archenteron, but
it permits the formation of mesenchyme. We might go on to
suggest that the early development of both Asteroidea and Echinoidea
is made up of the same processes, but that in the case of the
Echiuoidea the mesenchyme development is hurried on. In this
case it is not impossible that the hurrying on of the mesenchyme
formation in the blastula of Echiuoidea is due to the formation of
some substance which acts in a similar manner to the sulphocyanide,
and that, therefore, one main difference between the eggs of
Asteroidea and Echinoidea is the presence of this substance in the
latter type of eggs, and its absence in the former.

OPHIUROIDEA

Leaving now the Asteroidea, let us turn to the consideration of
the group most nearly allied to them, the Ophiuroidea. The develop-
ment of three species of Ophiuroids is known, viz. Opliiothrix fragilis,
Ophiura brevis2)ina, and Amphiura squamata. Of these only the
first possesses a long larval development comparable with that of
Asterias, and we shall therefore select it as type for special descrip-
tion. Its development has been worked out by us (1907).

Ophiura brevispina has a yolky egg and a much modified larva,
which takes no nourishment and creeps slowly about on the bottom,
and therefore exhibits a development in some respects parallel to
that of Cribrella and Solaster. Amphiura squamata has a develop-
ment which is passed entirely within a pocket in the maternal body
—the genital bursa — which acts as a womb, from which the
embryo emerges as a star-fish similar to the adult in all important
respects.

XVI

ECHINODERMATA

485

OPIIIOTHRIX FRAGILIS

Methods of preservation and staining which are applicable to
the study of Asterias are equally applicable in the case of Ophiothrix ,
and it will therefore be unnecessary to repeat them here. One
interesting point, however, remains to be noticed. The normal
development of the eggs of Ophiothrix fragilis was only obtained

arch

a. vac

long

blp

-pvac

FIG. 373. — Early stages iu the development of Ophiothrix fragilis. (Original.)

A, early blastula, seven hours old. B, yastrula, twenty-one hours old. C, Larva, thirty hours nld,
viewed from the ventral side, arch, wall of archenteron ; a. me, anterior vacuoluted crest; I'!'-, blastu-
coele ; Itlp, blastopore ; p.mes, primary mesenchyine ; ji.mr, posterior vacuolated crest.

in the case where these eggs were spawned naturally ; this was
accomplished by placing the males and females, which are easily
recognizable by the colour of the gonad shining through the skin,
in pairs, in separate vessels of clean sea-water. The females have
a colour which varies from light red to dark-brownish red, the males,
on the contrary, are of a light yellow or buff colour. The eggs are
very small, not more than -1 mm. in diameter, and are rendered
quite opaque by the dense accumulation of red yolk grains.

486

INVEETEBKATA

CHAP.

Segmentation takes place with great rapidity, and in four or five
hours a small spherical blastula, consisting of relatively few cells, is
formed. Then primary mesenchyme (p.mes, Fig. 373, A) becomes
budded off from one pole, and occupies a large portion of the
blastocoele. The side of the blastula from which this is budded off

a. vac

®

p.mes

arch

•p.mes

cce

al

p. vac

FIG. 374. — Longitudinal frontal sections of early larvae of Ophiotfi/rix fragilis. (Original.)

al, alimentary canal ; arch, archenteron ; u.nu; anterior vacuolated crest ; coe, rudiiiinit <>f coelom ;
/'.'.", postero-lateral arm; p.titcs, primary mesenchyme; j>. mo, posterior vacuolated crest; s.mes,
secondary mest'.ncliyme.

is of course the vegetative pole. The opposite pole of the blastula
develops into a great conical protuberance, which we may term the
anterior vacuolated crest. This arises (a.rac, Fig. 373, B) as a
consequence of the growth in height of the cells which form the
blastula wall in this region. They become changed into elongated
pillars, and develop clear vacuoles in their interior (a.vac, Fig. 374, A),

xvi ECHINODERMATA 487

and the vacuoles almost certainly consist of some material which
is lighter than water. Thus, while the general shape of the embryo
becomes conical, the outline of its cavity, the blastocoele, remains
spherical.

The blastnla now acquires cilia, bursts the egg-membrane, and
enters on a free swimming existence. Before eighteen hours have
elapsed the invagination to form the archenteron has begun, and
the blastula has become a gastrula. Secondary mesenchyme is
given off from the apex of the archenteron as this is being formed.
When the archenteron is fully formed it swells out at its free end
into a thin-walled vesicle, which is the rudiment of the coelom
(coe, Fig. 374, B). In Asterias, as we have seen, there is also formed
a single vesicle at the apex of the archenterou, but, according to the
current account, the coelom originates as two sacs which are cut off
separately from the archenteron.

In Ophiothrix, however, when this vesicle becomes cut off from the
archenteron, it persists for a brief time as a single vesicle ; then it
becomes divided into right and left halves, which lie at the sides of the

O '

gut and form the right and left coelomic sacs. At the same time two
lateral outgrowths of the body appear in the larva, which has up till
now had a conical shape (p.l.a, Fig. 373 C); these are the rudiments of
the postero-lateral arms, and into them passes nearly all the primary
mesenchyme. The cilia, which until now have covered the whole
body, become restricted to a circular band of thickened ectoderm
which passes over these arms. This band is, of course, homologous
with the longitudinal ciliated band of the Bipinnaria larva. In the
mesenchyme at the base of each rudimentary arm there appears a
little tri-radiate spicule of calcium carbonate. Of its three rays one
extends downwards towards the posterior pole of the larva, this is
termed the body-rod ; one extends outwards into the arm and is
termed the postero-lateral rod ; and the third extends in an anterior
direction and is termed the antero-lateral rod (a.l.a, Fig. 375, A).

The stomodaeum makes its appearance just behind the vacuolated
crest on what will prove to be the ventral side of the larva. As it is
being formed, the gut, from which the coelom has detached itself,
becomes marked out into three regions, viz. oesophagus, stomach,
and intestine, by the appearance of two constrictions. The
stomodaeum joins the oesophagus, and when this has been accomplished
the alimentary canal is complete. The opening of invagination, or
blastopore, persists as the larval anus. An adoral band of cilia is
formed just in the snme way as it is formed in the Bipinnaria, and
doubtless fulfils the same function. At the same time the two larval
arms grow rapidly in length, and the portions of the ciliated band
which pass over them are pulled out into long loops. The vacuolated
crest diminishes in size and soon disappears completely, and the whole
organism takes on in consequence the form of a V. The growth of
the larval arms appears to be due to the growth of the calcareous
rods contained in them, not because the growth of the arm is due to a

488

INVEKTEBEATA

CHAP.

passive stretching of the ectoderm, but rather because the pressure of
the growing tip of the rod stimulates the ectoderm to increased growth.
If the larva be exposed to unfavourable conditions, such as lack of
oxygen, etc., the ectoderm shrinks, and the pointed tip of the
calcareous rod projects as a naked spine, so that if there were any
stretching of the ectoderm the spine would immediately pierce it.
As the anterior vacuolated crest disappears, another, consisting of

'Hong

a

rcoe

rcce

b.r

FIG. 375. — Ventral views of young larvae of Ophiotl\ri.<- J '/•»'.</ His. (Original.)

A, larva, two and a quarter days old. B, larva, three days old. a, anus ; a.La, antero-lateral arm ;
a.l.r, antero-lateral rod; 6.?-, body rod; fil.lniii/, longitudinal ciliated band; iitt, intestine; t.i-oc, left
coelomic sac ; p.!.", jiostfro-lati'ral arm ; p.l.r, postcro-lateral rod ; p.o.a, post-oral arm ; p.o.r, post-
oral rod ; r.me, right coelomic sac ; st, stomach ; stum, stoinodauum.

a precisely similar ridge of ectoderm, makes its appearance at the
posterior pole of the larva, and this second crest persists through
the entire period of larval development. This we may term
the posterior vacuolated crest. The purpose of these crests
seems to be to diminish the specific gravity of the larva, and so
balance the increase in weight due to the development of calcareous
matter. The posterior rod of the calcareous star on each side meets
its fellow just above this posterior crest. The lower ends of
these "body -rods" bifurcate, and, by the meeting of the forks

XVI

ECHINODERMATA

489

a quadrangular calcareous frame is made. When the posterior
vacuolated crest is formed the anus becomes displaced on to the
ventral surface of the larva, and the whole alimentary canal becomes
curved so as to be
concave ventrally as in
the Bipinnaria larva.
The left coelomic sac
sends up a vertical out-
growth towards the
dorsal surface which
meets the ectoderm. At
this point the ectoderm
becomes vacuolated and
then perforated, and so
the primary madre-
poric pore is formed.
The outgrowth from the
left coelomic sac forms
the pore-canal.

Whilst these changes

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are going on another
pair of larval arms make
their appearance. These
are situated at the
sides of the mouth, just
where the lateral portion
of the ciliated band
passes into the anterior
cross-bar. They owe
their origin to the
stimulus provided by
the growth of the antero-
lateral rod and are
termed the antero-
lateral arms. There are
no appendages in the
Bipinnaria which exactly
correspond to these in
position.

The larva, not of
Ophiothrix fragilis, but
of the genus Oghiura,
in the four - armed con-
dition, was seen by

Johannes Miiller (1845). He thought it a new form of adult
marine animal, and named it Pluteus paradoxus, from the resemblance
it presented to a painter's easel (jiluteus] on four legs, when turned
upside down. Miiller, as a matter of fact, orientated the larva

—

to '

490 INVERTEBKATA CHAP.

wrongly. A year later, however (1846), he bestowed the same name
on the similar larva of an Echinoid, which, though generally homo-
logous with the larva of an Ophiuroid, differs from it in most
important points of detail. The confusion of having the term
" Pluteus " applied indifferently to both forms of larvae, led Mortensen
(1898) to propose that the single term Pluteus should be replaced
by the terms Ophiopluteus and Echinopluteus, as applied to
Ophiuroid and Echinoid larvae respectively, and this excellent
practice will be followed here.

When the larva has become endowed with a complete alimentary
canal it is able to feed, and it grows rapidly in size. The four arms
increase in length, but the first-formed pair, the postero-lateral, grow
very much more quickly than the others. The coelouiic sacs grow
in length and extend backwards along the sides of the oesophagus, and
beyond the junction of this with the stomach to the sides of the latter.

When the larva is about a week old important changes occur.
Two additional pairs of arms are developed ; of these one pair are
situated at the sides of the oesophageal region ; they correspond
roughly in position to the appendages of the Bipinnaria known as
postero dorsal, and receive the same name. The other pair arise in
front of the anus, from the posterior cross-bar of the ciliated band,
and are termed post-oral, since they correspond to the similarly
named appendages of the Bipinnaria. Each new arm is supported
by a calcareous rod which is developed as a new branch from one of
the two original calcareous stars. The rods supporting the post-oral
arms take their origin from the centre of the star, on each side, which
thus becomes quadri-radiate, but those supporting the postero-dorsal
rods spring, as branches, from the rods which support the antero-
lateral arms.

Whilst these changes have been occurring the coelom has been
undergoing further development. First on the left side and then on
the right, the coelomic sac becomes transversely segmented into
anterior and posterior divisions. The posterior divisions apply
themselves to the sides of the larval stomach, which has now become
globular ; thus these posterior divisions are somewhat widely separated
from the anterior divisions, which lie close to the larval oesophagus,
just over the region occupied by the posterior part of the ad oral
ciliated band.

It is obvious that the anterior part of each coelomic sac corre-
sponds to the anterior coelom of the Bipinnaria, and the posterior por-
tion to the posterior coelom of that larva. From the inner walls of
the anterior coelom on both sides are developed muscular fibres which
form a series of circular muscles surrounding the oesophagus, and by
which its peristaltic movements are carried out. All the arms grow
rapidly in length, but the postero-lateral outgrow all the rest and the
V form of the larva is maintained.

From the posterior ends of the right and left anterior coeloms a
thick-walled vesicle is nipped off. These are the rudiments of the

xvi ECHINODEEMATA 491

hydrocoele on the left and of a vestigial right hydrocoele

on the right ; they are at first quite similar to one another.
Nevertheless the left side of the larva is clearly distinguishable
from the right because the pore -canal opens on the left side, and
the portion of the anterior coelom into which it opens becomes dis-
tended so as to form an ampulla. This ampulla is connected with the
rudiment of the left hydrocoele by a narrow neck, which later forms
the stone-canal. On the right side the right hydrocoele remains
close to the right anterior coelom. Further, while the lumen of
the hydrocoele becomes enlarged, and the cells forming its wall
arrange themselves in a single layer of regular columnar epithelium,
the lumen of the right hydrocoele remains small and the cells remain
rounded and of irregular arrangement.

BIPINNARIA AND OPHIOPLUTEUS LARVAE COMPARED

The larva has now reached the height of its development, and
from this period may be dated the beginning of its metamorphosis
into the adult Ophiuroid. Before considering this it will be instruc-
tive to compare the Ophiopluteus larva, point for point, with the
Bipinnaria at a similar stage of development, vi/. just before the
appearance of the Brachiolarian arms.

The two larvae agree in the following points:—

(a) Both have a similar alimentary canal, consisting of a wide
shovel-shaped stomodaeum, cylindrical oesophagus (along the sides
of which and of tbe stomodaeum runs the V-shaped adoral ciliated
band), a globular stomach, and cylindrical intestine ending in ventral
arms. In both the alimentary canal is bent in a curve which is
concave ventrally.

(6) Both have a similar organ of locomotion, consisting of a
longitudinal ciliated band composed of two longitudinal sides and
anterior and posterior cross bars. In both this band is produced
into long arms or processes which extend its surface.

(c) In both the space between gut and skin is filled by a watery
gelatinous connective tissue.

(d) In both there are a pair of coelomic sacs which become
divided into anterior and posterior moieties ; and in both the rudi-
ment of the water-vascular system arises from the posterior end of
the left anterior sac, and into this sac the pore-canal opens.

On the other hand the Bipinnaria and the Ophiopluteus larva
differ in the following points :—

(«) The Bipinnaria has a long prae-oral lobe, and the loop of the
longitudinal ciliated band, which is bent along the ventral side of
this lobe, becomes separated from the rest as a distinct prae-oral band
of cilia. The prae-oral lobe is obsolete in the Ophiopluteus, and the
longitudinal ciliated band remains undivided.

(&) The processes of the ciliated band remain soft in the
Bipinnaria, and are usually short in comparison with the size of

492 INVEKTEBEATA CHAP.

the body ; they become, however, much longer iu other forms of
Bipinnaria than the one described. In the Ophiopluteus they are
very long in comparison with the size of the body, especially the
postero-lateral ones, and are supported by calcareous rods ; but in
other forms of Ophiopluteus larva they are not so long as in the
one selected as type.

(c) The two anterior coeloms extend into the prae-oral lobe in the
Bipinnaria, and fuse there into one anterior cavity ; also the septa
dividing anterior from posterior coeloms are formed late, and that on
the left side undergoes secondary perforations. In the Ophiopluteus
the right and left anterior coeloms remain separate, and the septa
dividing them from the right and left posterior coeloms are formed
early and are not subsequently perforated.

(d) A vestige of the right hydrocoele is formed in the normal
Ophiopluteus larva, but in the Bipinnaria larva this only occurs as a
variation.

On reading over the above comparison it is obvious that, if the
fully grown larvae of wisterias glacialis and of Ophiothrix fragilis
were met with for the first time, and were mistaken for adult
animals, they would be regarded as genera belonging to the same
family. The existence of such a deep-seated fundamental resemblance
points to the former existence of a simply organized, bilaterally
symmetrical, free-swimming, common ancestor of Asteroidea and
Ophiuroidea. Our faith in the former existence of. this ancestor will
be further strengthened when we have examined the development of
the three remaining classes of Echinodermata.

METAMOKPHOSIS OF OPHIOTHRIX FRAGILIS

Stage A. — The metamorphosis of Opliiothrix fragilis is initiated,
just as is that of Aster ias glacialis, by a preponderate growth of the
organs of the left side, viz. the left hydrocoele and the left posterior
coelom. The former of these grows long and extends forwards, along
the oesophagus, completely overlapping the left anterior coelom. At
the same time it becomes divided into five lobes by constrictions
which appear on its inner side. These are, of course, the rudiments of
the five radial water-vascular canals and of the azygous tentacles or
tube feet in which they terminate (Fig. 377, C). By this growth the
original posterior end of the stone-canal is pulled forwards, so that it lies
in front of what was originally the anterior end. A madreporic
vesicle is formed, apparently in the same way as in Asteroidea.

The left posterior coelom also extends forwards. Its inner wall
remains thin, but its outer wall begins to develop great proliferations
of cells which form conical protuberances. Into each conical pro-
tuberance a narrow diverticulum of the lumen extends. These
protuberances, which raise corresponding humps in the ectoderm, are
the rudiments of the adult arms.

As the left hydrocoele increases in length its anterior end begins

XVI

ECHINODEKMATA

493

to extend over the dorsal surface of the stoinodaeum, and its posterior
end sweeps round to the right, across the ventral surface of the

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oesophagus. In this way it is gradually transformed into a circle,
the two ends of which meet on the right side of the mouth, which
thus becomes completely surrounded. The lobes project into the
stoinodaeum as tentacles covered by stomodaeal ectoderm. This

494

INVERTEBRATA

CHAP.

growth of the left hydrocoele is accompanied hy a growth of the
whole left side of the larva. Thus we find that by this growth the
left antero-lateral larval arm is carried across to the right side, so as
to lie close to its right partner, whilst the left postero-dorsal arm is
carried forwards to a position where it might easily be mistaken for
the left antero-lateral arm (Fig. 377, C).

The left anterior coelom and its pore - canal are also carried
forwards till they reach the mid-dorsal line, in other words, till they
reach a position similar to that which they reach in the Asteroid

irit

Ip'c

p.vac

FIG. 378. — Longitudinal frontal section of a larva of Ophiothrix fragilis, in the first
stage of metamorphosis. (Original.)

3, 4, 5, third, fourth, and tifth primary lobe of the hydrocoele respectively, eji.f, epineural fold ;
tut, intestine; l.p.c, left posterior coelom; ?ij»ifi, right ventral horn of the left posterior coelom; 'ji.li. 3.4,
/>./(. 4.0, perihaemal rudiments intervening between lobes 3 and 4, and lobes 4 and 5, respectively, of the
hydrocoele ; p.nv, posterior vacuolated crest ; *Y, stomach ; stum, stomodaeum.

larva at the same stage. The left posterior coelom sends out a right
ventral horn (llplcl, Fig. 378) which sweeps over to the right side,
beneath the oesophagus, and eventually meets the horn of the same
cavity which has extended dorsal to the oesophagus, thus forming a
complete ring. Two of the arm rudiments are formed from this
horn, the other three arise from the main part of the left posterior
coelom.

From the inner side of the left posterior coelom there are given
off wedge-shaped, thick-walled evaginations, which alternate with
the lobes of the hydrocoele and extend ventrally to them. These are
the rudiments of the perihaemal ring-canal, and of the radial

xvi ECHINODEEMATA 495

perihaemal canals, which are thus formed in a manner similar to
that described for Asterias. One of these rudiments arises from the
left anterior coelom.

The main difference between these perihaemal rudiments and the
corresponding structures in the Asteroid larva is, that in the
Ophiuroid they are thick-walled and their cavities are mere slits
(r>.h, Fig. 378), whereas in Asterina gibb'osa, at any rate, they are
thin-walled and open by wide mouths into the coelom.

On the stomodaeal ectoderm, just over the places where these
perihaemal rudiments are situated, five ridges make their appearance
which radiate inwards towards the centre of the mouth. The crests
of these ridges give off diverging lamellae to right and left, which
may be termed epineural flaps (ep, Fig. 378). These lamellae meet
those of adjacent ridges, and thus form roofs over the basal portions
of the lobes of the hydrocoele, i.e. those portions which will form the
radial canals. In this way is formed the epineural roof which covers
in each radial nerve cord of the adult.

Stage B. — The changes which have just been described go on
simultaneously, and constitute what we may call stage A of the
metamorphosis. In the next stage, which may be termed stage B,
further changes supervene and the absorption of purely larval organs
commences.

All the larval arms, except the two poster o- lateral, become
reduced in size, the ectoderm covering them retreats to their bases
and is devoured by phagocytes, and the spines of the larval skeleton
are exposed and broken off. In the meantime the lobes of the
hydrocoele each develop two pairs of lateral lobes, the rudiments of
the first two pairs of tentacles representing the paired tube feet of
Asteroidea (6.*, Fig. 379).

The perihaemal spaces extend outwards, — i.e. as in Asteroidea,
the adjacent sides of two neighbouring perihaemal spaces become
apposed to form the two radial perihaemal canals of each arm,
which later fuse into one. Branches of these canals extend along
the surfaces of the lateral tube feet.

The outer part of the stomodaeum, which enclosed the primary
lobes of the hydrocoele, shallows out and disappears. The adult
mouth is formed about the spot where stomodaeum and endodermal
oesophagus meet one another ; in a sense it is identical with the larval
mouth, because it is, as it were, formed from the deepest recess of the
structure, but it cannot be too strongly emphasized that in Ophiuroids,
as in Asteroids, the stomodaeum is a temporary structure.

In the Asteroid the adult mouth is formed to the left of where the
larval mouth and stomodaeum were situated. Now, in Ophiothrios, in
this stage, the stomach and intestine are displaced to the right, and
this is obviously the same as saying that the mouth moves to the
left, because in speaking of the Asteroid the stomach and intestine
are taken as fixed points. If we were to regard the outer end of the
endodermal oesophagus in the Asteroid, i.e. the inner end of the

496

INVERTEBRATA

CHAP.

stomodaeum, as homologous with the adult mouth of an Ophiuroid,
then we might say that in the Ophiuroid this point is displaced ~by

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growth towards the left side, whereas in the Asteroid it disappears and
is replaced by a new growth farther to the left. Therefore the Asteroid in
this respect obviously exhibits a more modified course of events, and

XVI

ECHINODEEMATA

497

to this extent the development of an Ophiuroid is more primitive
than that of an Asteroid.

Stage C. — In the next and concluding stage of the meta-
morphosis, which we may designate stage C, all trace of the larval
arms, except the two postero-lateral, has disappeared. The adult arms
have, however, grown in length and have become apposed to the lobes
of the hydrocoele. This apposition is brought about by the shrinkage

st p.o.c Ipc

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'mp
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ten

m.v

ep

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. 380. — Transverse sections through the discs of two young brittle-stars in order to
show the origin of the germ cells. (Original.)

A, section through young Ophiothrix fragilis juat after metamorphosis. B, section through the
embryo of Auipltium squumata '25 mm. across the disc taken from the maternal brood pouch, amp,
ampulla, the derivative of the left anterior coelom ; ep, epineural space ; germ, primitive germ cells ;
J.p.i; left posterior coelom; m.p, madreporic pore; m.r, madreporic vesicle; n.r, nerve ring ; ph. I. '2,
pcrihaemal space, derived from the left anterior coelom (ampulla) and still opening into it ; p. <>.<•, peri-
oral coelom ; p. «<<•, posterior vacuolated crest ; st, stomach ; st.c, stone-canal.

of the ectoderm connecting the two structures. The outline of the
young Ophiuroid, instead of being merely pentagonal, as it was in
the preceding stage, has become definitely five-rayed, but the rays
are folded inwards underneath the disc.

There is found as an outgrowth of the left posterior coelom, a

peri-oral coelom (p.o.c, Fig. 380), corresponding to that found in

Asteroids, which interposes itself between the left posterior coelom

and the oesophagus. This appears to persist throughout life in the

VOL. I 2 K

498 INVEETEBRATA CHAP.

Ophiuroid. In the Asteroid, as we have seen, the dividing wall
between the peri-oral and the left posterior coelom breaks down and
leaves as remnants the ten " retractors " of the stomach. The
intestine and larval arms have by this time completely disappeared.

From the walls of the radial perihaemal spaces proliferations of
cells take place. Those on the ventral side of these spaces are
apposed to the thickened bands of ectoderm which form the radial
nerve cords, and they constitute the coelomic ganglia, which are the
motor elements in the nervous system. From the dorsal walls of
these spaces masses of cells are given off which form the great
longitudinal muscles connecting the " vertebrae " of the arm. From
the sides of the arms movable hooks are developed (h.k, Fig. 379).
These hooks are found, in the adult Opliiotlirix, ventral to the
transverse rows of arm spines, and are characteristic of the genus.

By this time the metamorphosing larva has reached the bottom,
and it commences to walk on its tube feet. The postero-lateral arms
shrink, the flesh retreating to their bases and the spines becoming
exposed. The naked spines are soon broken off and the young brittle-
star walks away. Very soon its arms have become so long that the
wriggling movements, so characteristic of the adult, supersede the
action of the tube feet.

AMPHIURA SQUAMATA — SKELETON AND GENITAL ORGANS

The development of the calcareous skeleton and of the genital
organs has not been followed out in Ophiothrix, but has been worked
out in the species Ampliiura squamata. As mentioned above, this
animal carries the young about in its genital bursae until they
resemble the parent in all points except size and the development of
the genital organs. It is hermaphrodite, one testis and one ovary
discharging into each bursa.

Eusso (1891) has given a general account of its development, but
as this worker did not employ the method of sections to any great
extent, and as the young stages are met with seldom and are very
opaque, it is quite likely that his account is inaccurate. According to
Eusso the blastula is converted into a two-layered gastrula by delarni-
nation (!), each cell dividing into an inner endodermic and an outer
ectodermic portion, and the coelom is said to arise as splits in
a mass of mesenchyme. Such statements as these are improbable in
the highest degree. The embryo is oval without any of the outgrowths
characteristic of the Ophiopluteus ; it has, however, a larval skeleton,
consisting of a network of calcareous trabeculae, which is absorbed
before the metamorphosis is complete. This network arises as two
calcareous " stars " which arise in the mesenchyme to the right and
left of the alimentary canal, and which branch, and their branches
unite to form the network. Even before the pentagonal form is
attained the rudiments of the adult plates begin to appear.

The most satisfactory account of the development of these plates

xvi ECHINODERMATA 499

has been given by Ludwig (1881), but Fewkes (1887) has also
published a paper on the subject. We find on the aboral side of the
larva a central plate, the so-called dorso-central, which is surrounded
by five plates which are iuterradial in position. One of these plates
surrounds the madreporic pore, which is thus at first situated at the
edge of the dorsal surface, not on the oral surface, where it is found in
the adult. Fewkes terms these plates basals. Alternating with
these are found a circle of five so-called radials, not to be confused
with the radial shields of the adult, a pair of which occur above the
insertion of each arm. Farther out, overlying the tips of the lobes
of the hydrocoele, grooved plates, concave below, represent the
terminals. These plates protect the terminal tentacle which is formed
from the tip of the primary hydrocoele lobe. Later they become
converted into cylinders by the meeting of the edges of the groove.

On the oral side, alternating with the tube feet or secondary lobes
of the hydrocoele, spicules of calcareous matter make their appearance.
These are Y-shaped, the stern of the Y being directed towards the
point of the arm and the fork towards the mouth. The fork is really
the beginning of a system of dichotomous branching, by which a
mesh work is produced, since the members of further dichotomies unite
with one another just as has been described in the formation of an
Asteroid plate. A similar process of dichotomy begins later in the
end of the stem.

In this way each Y forms a narrow plate, elongated in the
direction of the arm. The proximal ends of the right and left plates
unite with one another first, and then the distal ends. In this way
the beginning of a vertebra is formed. It is obvious that the two
plates correspond to the ambulacral plates of an Asteroid. In the
genus Opliiolidus the " vertebrae " consist throughout life of two rods
joined at either end with a hole in the middle, just as they are in the
young Amphiura squamata.

Other plates are formed on the sides of the arm, these are
lateral plates or adambulacrals, and on the aboral side other plates
make their appearance. Between dorso-central and so-called basal,
on each interradius, two plates appear. These force the basal round
to the ventral side of the young star-fish, and their appearance is
therefore correlated with a growth in length of the interradii ; the
radii grow more slowly.

A plate, the so-called underbasal, becomes interposed between the
radial and the centro-dorsal, but the radial is not forced far out or on
to the ventral surface. On the contrary the greatest growth takes
place between the radial and terminal, and is correlated with the
growth in length of the arm. The true " radial shields " appear as
paired plates between the embryonic radials and the terminals. The
first two pairs of auibulacrals do not unite with one another, but each
unites with the first adambulacral or lateral, and this forms half the
jaw-frame, the other half being formed by the similar plates in the
next ray.

500

INVEETEBRATA

CHAP.

While these developments are going on in the skeleton the
foundations of the genital system are being laid. The development
of this has also been worked out by us (MacBride, 1892). It will be
remembered that the madreporic pore, and of course the pore-canal and
left anterior coelom along with it, are forced from a marginal to a
ventral position owing to the growth of the interradius. The original
mesentery separating oral from aboral coeloms, i.e. left from right
posterior coeloni, is largely perforated, but it too persists and extends
from the stomach obliquely downwards instead of upwards. The stone-
canal also extends obliquely downwards, and where the wall of the

FIG. 381. — Two diagrams to elucidate tho mutual relationships of stone-canal, dorsal organ,
axial siuus, madreporic vesicle, genital rachis, etc., in an Asteroid and an Ophiuroid
respectively.

A, relations of these organs in an Asteroid. B, relations of these organs in an Ophiuroid. <ib.s,
aboral sinus ; aid, space derived from the anterior coelom — in A termed axial sinus, in B ampulla ; tl.u,
dorsal organ ; gen.r, genital rachis ; m.p, madreporic pore ; ?»..!•, madreporic vesicle ; p.g.itii', primitive
germinal imagination — this space disappears in A, but in B forms the so-called axial sinus ; st.c, stone-
canal. The arrow shows the direction in which the structures in A must be rotated to reach the con-
dition in IJ.

left posterior coelom abuts on it one can observe that the nuclei
of the latter become enlarged.

This is the first indication of the primitive germ-cells, and forms
the genital stolon tissue, constituting the dorsal organ. It becomes
protected by the outgrowth of a covering flap which grows down from
the central end of the stone -canal. The space left between the
primitive germ-cells and the cover-flap has been confused with the
axial sinus of Asteroidea, and has received the same name ; it is,
however, quite distinct from this, and corresponds to the cavity
of the primitive germinal involution of Asteroidea, which soon
closes ; the corresponding cavity in Ophiurids persists for life.

xvi ECHINODERMATA 501

The genital rachis grows out from the peripheral end of the
stolon, ami the aboral sinus surrounding it arises by the development
of a covering flap, just as happens in Asteroidea. The genital rachis
pursues an undulating course, being situated aborally where it crosses
the radii and ventrally in the interradii. As it slopes downward
from radius to interradius it passes over the surface of the genital
bursae, which develop as invaginations of the ectoderm. Here the
genital organs develop as buds, which press against the bursa and
form their own openings into it at maturity. Thus all the parts
which can be recognized in the genital system of Asteroids are repre-
sented in Ophiuroids, but the aboral end of the stone-canal has been
rotated downwards (Fig. 381).

OPHIURA BREVISPINA

The development of Ophiura brevispina (1900) has been worked
out by Caswell Grave. The egg is comparatively large and very
yolky ; and development is rapid, the metamorphosis being complete
in ten days. The development bears somewhat the same relation to
that of Ophiothrix as that of Solaster does to Asterias. The earliest
stages were not observed, but it appears that a blastula is formed, the
cavity of which becomes filled with precociously formed mesenchyme.
Then an invagination of a solid mass of cells takes place, which
becomes hollowed out so as to form an archenteron, in such a way
that, for a time, a solid tongue of cells projects into its cavity.

The gastrula rapidly elongates, and there is formed in front of the
archenteron a long head region filled with mesenchyme. From the
apex of the archenteron a coelomic vesicle is cut off, which soon
divides into right and left sacs ; these form the right and left anterior
coeloms. At the same time the rest of the archeuteron becomes cut
by a circular furrow into a small dorsal sac, which forms the stomach,
and large ventral one, the front part of which forms the hydrocoele
and the hinder part the posterior coelom. The mouth arises as a
wide shallow invagination on the ventral surface, while the hydro-
coele rapidly develops its five lobes and grows round it.

The external form of the larva is now cylindrical, but slightly
thicker behind than in front. The universal coat of cilia has given
place to five transverse rings of cilia, which give the creature the
appearance of being segmented and led Johannes Miiller, by whom it
was first discovered, to call it the "worm-like larva." It glides
slowly over the bottom. Soon the hydrocoele ring becomes completed
and the azygous tentacles appear as external protrusions, and in this
way a pentagonal figure is outlined on the under side of the posterior
part of the larva.

Although the hydrocoele arises from a rudiment common to the left
posterior coelom, it becomes cut off from this and forms a secondary
connection with the left anterior coelom, which is the stone-canal.
Only after this has occurred is the pore-canal formed. The larva now

502

INVEETEBKATA

CHAP.

looks like a young Asteroid, and for this reason Johannes Miiller
included the " worm-like larva " amongst the Asteroid larvae.

As development proceeds the anterior part of the larva diminishes
in size, and the adult arms grow out. The epineural spaces appear
at first as open grooves, the edges of which meet. The perihaemal
spaces arise exactly as in Ophiothrix.

The only strikingly abnormal features about this development are
the method of the gastrulation and of the formation of the coelom.
With regard to the first point, it is a remarkably interesting fact that
if the eggs of Ophiothrix be removed from the ovary and artificially

fertilized, instead of being
allowed to be spawned natur-
ally, they often exhibit the
same kind of early develop-
ment as Grave has described
for Opliiura brevispina. The
mesenchyme begins to be cut
off in the early stages of
segmentation, so that the
blastocoele, from its very
beginning, is filled with it,
and the blastula is in reality
a " morula." Invagination is
a solid inwandering of cells,
and, when this solid mass
becomes hollowed out, a
tongue of cells persists which
projects into the lumen of
the archenteron. Such larvae
never develop the anterior
vacuolated crest.

This interesting fact leads
us to form some such con-
clusion as this. The processes
of growth and cytotaxis, which
are the underlying causes of

the outward and visible "signs" of formation of mesenchyme, in-
vagination, etc., are the same over a wide range of species. The
relations of these processes to each other in degree of intensity
and times of maximal intensity, in a word the differential equations
which connect them, differ as we pass from species to species, and in
consequence the same processes give rise to very different visible
results in different cases. By interfering with the normal relations
in any one species, in the case of Ophiothrix, by fertilizing the egg
before it is quite ripe, the conditions usually found in quite a different
species may be reproduced.

With regard to the formation of the coelom, we have learnt how
profoundly this process may be altered amongst Asteroidea by the

FIG. 382. — Ventral view of the larva of Ophiura
brecis during the metamorphosis. (After
Grave. )

as.?, rudiment of azygous tentacle; b.t, rudiments
of buccal tentacles ; cil, transverse ciliated bands ;
u, mouth.

xvi ECHINODERMATA 503

presence of yolk, and so we are the less surprised at its abnormality in
Ophiura. But it should be added that Grave had only a limited
amount of material to work on, which he could not augment as
second attempts at artificial fertilization did not succeed. Hence it
is possible that some of his interpretations may be mistaken.

DEVELOPMENT OF OFHIOTHRIX AND ASTERIAS COMPARED

When we compare the development of OpMothrix with that of
Asterias we notice two main differences : first, the fixed stage is dropped
out completely ; the Ophiuroid, by the retention of the postero-lateral
larval arms, is enabled to pass through its metamorphosis floating ;
and, secondly, some of the larval changes are simpler and more direct
in character than in Asterias. Thus the segmentation of the coelom
is not complicated by subsequent perforations of the septum, and the
larval mouth persists. The perforations of the septum seem to be
due to the body musculature developed in Bipinnaria, which renders
it necessary to allow the coelomic fluid to pass from one part to
another. It is hardly likely that, in the primitive condition of
affairs, if a segmentation took place it would be largely undone
immediately afterwards, so that in this respect Opliiothrix is prob-
ably more primitive than Asterias.

Then, as to the retention of the larval mouth in the adult, there
can be no question that this more truly represents the history of the
race than the obliteration of the old mouth and the formation of a
new one in a new place. It is not easy to picture an animal in the
condition of losing an old mouth and gaining a new one. We have
seen that when the hydrocoele ring is just complete there is no epi-
neural fold developed, so that the nerve cord is exposed ; and further,
that when metamorphosis is just complete the animal walks on its
tube feet instead of using its arms. Young specimens of Amphiura
squamata, if cut out of the bursa of the parent when the arms are as
yet undeveloped, walk also on their tube feet, so that in these two
respects the Ophiuroid may be said to pass through an Asteroid stage.

Now there are found in Silurian and Devonian rocks a consider-
able number of fossils exactly intermediate in character between
Asteroidea and Ophiuroidea. We have every reason to believe that
in these fossils we possess the actual record of the evolution of the
Ophiuroidea, and we are therefore in a position to test how far
the history of the individual, as disclosed by embryology, agrees with
the history of the race. Now these fossils show an open ambulacral
groove, and ambulacral ossicles not yet united to form vertebrae, but
in the larva the open ambulacral groove becomes closed long before
there is any trace of vertebrae, and while the adult arms are still
mere stumps.

Hence we conclude that in the larval history there has been a
dislocation of the sequence of events, and that the formation of the
epineural flaps has been hurried on long before its time — in a word,

504 INVEETEBEATA CHAP.

that these flaps have been precociously developed. In dealing with
the development of Gastropoda, it will be remembered we saw reason
to believe that, in the veliger stage, we had an example of the
opposite phenomenon, viz. the retention of a larval organ long
beyond the stage when, according to ancestral history, it ought to
have disappeared.

ECHINOIDEA

The complete life -cycle has been described in a very few
Echinoidea. We possess records of the external appearance of the
larva in all stages of development in the case of Echinus miliaris
and Echinus esculentus, two species of regular Endocyclic urchins ;
also in the cases of Echinocyamus pusillus and Mettita testudinata, two
Clypeastroids ; and of Echinocardium cordatum, a Spatangoid. In
the case of Echinus esculentus the development has been thoroughly
investigated by us by means of sections (MacBride, 1903), and we
shall select this species as a type for detailed description.

Owing to the fact that the ovaries and testes in Echinoidea are
larger in proportion to the body and more compact than in any
other class of Echinodermata, a very large proportion of the ex-
periments, on which the science of "Experimental Embryology " is
founded, have been performed on the eggs of Echinoidea. With
hardly an exception, however, the experimenters have confined their
attention to that part of the development which terminates in the
formation of the four-armed larva ; and further, the overwhelming
majority of the experiments have been performed on the three
species most commonly found at Naples, viz. Echinus microtuberculatus,
Strongylocentrotus lividus, and Sphaerechinus granularis. All three
are regular urchins, and, in all important points, all three have given
identical results in the hands of experimenters.

When we reflect that Echinus microtuberculatus is only a local
race of Echinus miliaris, and that, except for insignificant details, the
early development of Echinus miliaris and Echinus esculentus is the
same, and that the development of Strongi/locentrotus lividus, which
has recently been investigated by von Ubich (1913), seems to be in
all respects similar to that of E. miliaris, we shall, without hesitation,
apply to Echinus esculentus the minute knowledge of the earliest
stages of development which has been gained by the concentration
of the attention of the experimenters on the Neapolitan species.

We shall first describe the normal development and then briefly
sketch the principal results arrived at by experiment.

The eggs of Echinus esculentus can be made to develop through
their complete life-cycle even when artificially shaken out of the
ovary. It is by no means necessary to wait for a natural spawning
in order to get good results. Echinus esculentus is a gregarious
form and can usually be obtained in large numbers, either by
dredging at moderate depths, as in Plymouth Sound, or by picking
it off the rocks at low tide in more sheltered situations, as in the Clyde.

xvi ECHINODERMATA 505

On the east coast of North America we find the species
Strongylocentrotus droebachiensis under similar conditions in count-
less thousands, and as the larva of Strongylocentrotus cannot be
distinguished from the larva of Echinus by any certain mark, all
that will be said about Echinus esculentus may be taken as apply-
ing to Strongylocentrotus. On the Pacific coast Strongylocentrutas
droebachiensis is replaced by the larger species S. purpiiratus and
S.franciscanus, the eggs of which are equally suitable for rearing.

METHOD OF OBTAINING NORMAL EMBRYOS

The urchins are most easily opened by inserting one blade of
a pair of scissors through the margin of the peristome, and then
cutting along a meridian of the shell till the equator is reached ;
the cut is then carried completely round the equator and so the
shell is separated into an upper and a lower half. In the upper
half will be found the genital organs.

The ripeness of the testes can be ascertained by squeezing out
a drop of the spermatic fluid into a drop of sea-water, when a
glance at the mixture through the low power of a microscope will
show whether the spermatozoa are active or not.

The ripeness of the eggs can be gauged by two criteria : (1)
whether they break loose from the ovary at the slightest touch, so
that the ovary appears to dissolve into dust ; (2) whether the large
germinal vesicle, so characteristic of the unripe egg, has dissolved.
Bolton cloth of a mesh of -i- mm. is a useful adjunct. If a piece of
ovary be wrapped in a piece of this cloth and shaken into clean
sea-water, the eggs, which easily detach themselves, will escape
through the meshes of the cloth, and the younger undeveloped ova
and follicle cells, which adhere to one another, will remain behind.

A better method of obtaining ripe eggs, however, is to invert
the upper half of the bisected urchin in a small glass dish containing
some sea-water. The ripe eggs will then be discharged practically
without admixture of unripe ones, an admixture which it is impossible
to avoid when pieces of the ovary are shaken out into sea-water.

If the eggs are perfectly ripe they will be free from all mem-
branes ; but they show a thick glassy chorion, just like that which
we have described in the eggs of Asterias glacialis, which prevents
the easy access of spermatozoa. If, however, these eggs are allowed
to lie for two hours in clean sea-water before being fertilized, the
chorion will completely disappear. Fertilization can, however, take
place before the chorion disappears.

In fertilizing, care must be taken that the eggs are spread out
over the bottom of the vessel in a single layer, and that a very
small quantity of spermatozoa is added. In practice, an emulsion
of spermatozoa is prepared by shaking up a drop or two of thick
spermatic fluid with sea-water in a specimen tube four or five
inches long. If the eggs are contained in a glass evaporating dish

506 INVERTEBEATA CHAP.

of the usual size (say eight inches in diameter), it is sufficient to acid
half a dozen drops of this emulsion to ensure fertilization of every
egg, if the mixture be thoroughly stirred up.

When once the eggs have fallen to the bottom, the supernatant
fluid, which contains the superfluous spermatozoa, must be decanted
off. Fresh sea-water is then added, and the eggs stirred up in it,
and the decantation repeated. In this way all the unused
spermatozoa are removed ; if this is not done they die and befoul
the water and impede the development of the eggs. Whether the
fertilization has been successful or not can be determined by
examining a sample of the eggs under a microscope half an hour
afterwards. It will be then seen that all the eggs which have been
ready to receive a spermatozoon have formed fertilization membranes,
between which and the egg there is an accumulation of fluid.

In eighteen to twenty-four hours the larvae will have burst these
membranes, and will be found swimming at the surface of the water.
They can then be decanted off into vessels filled with sterilized sea-
water (prepared as described under Asteroidea), and supplied with food
in the form of a pure culture of the diatom Nitschia, when they will
metamorphose into young sea-urchins in a period varying from six
weeks to two months. Too many larvae must not be reared in one
jar. In practice it is found that twenty or thirty is the largest
number which will thrive in a half-gallon jar. Direct sunlight is
to be avoided, and the larvae seem to do better when contained in
a jar made of green bottle-glass.

The methods of preservation, both for whole mounts and sections,
are the same as those prescribed for the larvae of Asterias and
Ophiothrix.

ECHINUS ESCULENTUS

The egg divides into two and then four equal cells, and the
8-cell stage is reached by the division of the four cells into two
tiers of four each. These cells touch each other laterally ; eventually
they are separated from one another by a space, the blastocoele. As
development goes on the blastocoele enlarges.

Then the 16 -cell stage follows. This is reached by the
members of one tier dividing, each into a very small cell below,
termed the micromere, and a larger one above, the macromere.
Each of the members of the other tier divides by radial cleavage
into two equal cells, and so a circle of eight cells of intermediate
size is formed. These are termed mesomeres. Driesch's experi-
ments (1900) have demonstrated what Boveri showed to be the
case by direct observation in the egg of Strongylocentrotus iividus
(1901), viz. that the micromeres are situated at the vegetative pole
of the egg, not at the animal pole as had been previously imagined.

In the next cleavage each micromere buds off a smallest
micromere, and the other cells divide into daughters of equal size.
In subsequent cleavages each of the smaller micromeres divides

XVI

ECHINODERMATA

507

once and then stops, whilst each of the larger micromeres divides three
times, giving eight cells. Each macroniere and each uiesomere
divides tive times, giving in each case sixty-four cells.

When these divisions have been accomplished each cell acquires
a cilium, and the hollow sphere of cells begins to rotate within the
egg-membrane, which it soon bursts. It then rises to the surface of
the water as a free-swimming blastula.

If the description of the cleavage of the egg, which has just been
given, has been correctly followed, it will be seen that the blastula con-
sists of 4 x 2 (smaller micromeres) + 4x8 (larger micromeres) + 4 x 64
(macromeres) + 8 x 64 (rnesomeres) cells, i.e. SOS cells altogether.
The blastula soon becomes flattened at the vegetative pole, and the
cells here begin to divide and to give off primary mesenchyme into
the blastocoele, just as happens in the case of the larva of Ophiotlirix

mesm

macm

mi cm

FIG. 383. — Two stages in the segmentation of the egg of Strongylocentrotus Jicidtis. (The
segmentation of the egg of Echinus esndcntus pursues an identical course.) (After
Boveri. )

A, 10-cell stage. B, 3^-cdl stage, mucnt, macroim-re ; inesm, mi'somere ;

i, micromere.

fragilis. This mesenehyme originates, almost certainly, from the
descendants of the smaller micromeres. Only a limited number
(fifty or thereabouts) of these mesenchyme cells are formed ; they
arrange themselves in a ring round the periphery of the blastocoele,
the plane of which is parallel to the plane formed by the vegetative
surface.

In two places, diametrically opposite to each other, the ring is
thickened and consists of a heap of cells ; elsewhere it consists of a
single line of them connected with each other by pseudopodia. In
the centre of each heap a little triradiate calcareous spicule appears;
these heaps of cells and their contained spicules are the first organs
which indicate the future bilateral symmetry of the larva.

Then the blastula becomes a gastrula by the invagiuation of the
archenteron, which begins in the centre of the flattened surface. As
in Ophiothrix and Asterias the archenteron is a narrow tube of small
diameter compared with the gastrula, but it reaches nearly to the

508

INVERTEBKATA

CHAP.

anterior end of the larva. No vacuolated crests of any kind are
developed, but with this exception the subsequent development, up
to the age of six days, is, point for point, identical with that of
Opliiothrix. The separation of the coelom from the archenteron,
its division into two sacs, the formation of the madreporic pore,
the formation of the stouiodaeum, the differentiation of the gut,
the formation of the adoral band of cilia, and of the longitudinal
locomotor band of cilia, of the first four larval arms, and of their
supporting calcareous rods, take place in precisely the same way as
in the Ophiopluteus larva and need not be specially detailed here.
No wonder that the Echinoid larva, when discovered by Johannes

coe

p.mes

arch

~calc

FIG. 384. — Early stages iu the development of Echinus esculentus. (Original.)

A, blastula. B, advanced gastrnla, showing the formation of the coelom. nrdi, archenteron ; Wp,
blastopoiv ; m/< , calcareous star ; ciY, apical tuft of specially long cilia ; coe, coelomic vesicle arising as
an outgrowth from the archenteron ; JJ.WHW, primary mesenchyme cells.

Miiller, was regarded by him as another species of his genus " Pluteus."
It is now termed Echinopluteus in order to distinguish it from the
Ophiuroid larva. The sole differences between the two which can
be detected at this stage concern — (1) The posterior ciliated arms;
these are more closely approximated to one another than in the
Ophiopluteus, and, as subsequent development shows, correspond to
the post-oral arms of that larva, not to those which are just formed
iu the Ophiopluteus, i.e. the postero - lateral. The Echinopluteus
in this stage is consequently rather more square in section — not so
flattened, in tact, as the Ophiopluteus. (2) The body -rods ; these,
instead of ending in the aboral pole in bifurcations, as is the case in
the Ophiopluteus larva, end in inbent crooks, which may branch
slightly but which do not unite with their fellows on the opposite
side of the body.

XVI

ECHINODERMATA

509

In a well-developed larva of this age, the body consists of a
conical mass which contains the larval stomach and intestine,
and from which spring the post-oral arms, and of an oral lobe
containing the mouth and oesophagus, from which spring the antero-
lateral arms.

The development during the second week of larval life presents
many resemblances to the development of the Ophiopluteus. Thus
the coelomic sacs divide into anterior and posterior portions, the
latter applying themselves to the stomach and the former to the
oesophagus, to which they supply constrictor muscles. A pair of

B

slom

poa

coe

oes

cilad

r.coe

br

FIG. 385. — Young larvae of Ecliinus esculentus viewed from the dorsal surface. (Original. )

A, prism larva, three days old. B, four-armed Echinopluteus larva, seven days old. u.l.a, anterior
lateral arm ; n.l.r, antero-lateral rod; b.r, body-rod ; ril.ail, adoral band of cilia; ciU<nif/, longitudinal
band of cilia ; coe, coelomie vesicle ; h.r, horizontal rod ; l.cne, left coelomic sac.; oe.s, oesophagus ; p.ii.a,
post-oral arm ; p.o.r, post-oral rod ; r.coe, right coelomic sac ; st, stomach ; stvm, stomodaeum.

postero-dorsal arms are developed, but these, unlike their homologues
in the Ophiopluteus, are supported by calcareous rods developed from
spicules totally independent of the primary calcareous spicules.

About the end of the second week rudiments of a fourth pair of
arms appear ; these are situated at the sides of the loop of the
longitudinal ciliated band which overhangs the mouth, the prae-oral
loop in fact. These are the prae-oral arms ; they are supported by
the forks of an independent V-shaped calcareous centre termed the
dorsal arch, which is situated in the mid-dorsal line above the
region of the oesophagus.

The larva has thus five independent calcareous centres and eight

510

INVEETEBEATA

CHAP.

arms. These arms are capable of movement, and can be slowly approxi-
mated or divaricated. These movements are due to muscular strands
connecting the rods near the aboral pole, and to others going out
to them from the ends of the oesophagus. Both sets are derived
from cells of the secondary niesenchyme.

When it is about twelve days old the left anterior coelom buds off a

inp

FIG. 386. — Echinopluteus larva of Echinus esculentus about eleven days, viewed from the
dorsal surface to show the formation of the ciliated epaulettes. (Original.)

Names as in previous figure. In addition, n.ril.e.p, anterior ciliated qiMiilrtti? ; urn, amniotic in-
vagination ; d.a, dorsal arch; liy, hydrocoele ; Ln.c, left anterior coelom ; LI'.'-, left posterior coelom;
in.p, madreporic pore; -111.1', madreporic vesicle ; p.c, pore-canal; ji.d.a, postero-dorsal arm; p.d.r,
postero-dorsal rod ; -pr.u.a, prae-oral arm ; r.a.c, right anterior coelom ; r.p.i; right posterior coelom ;
st.c, stone-canal.

posterior vesicle, which remains connected with it by a narrow neck.
The vesicle is the hydrocoele which gives rise to the adult water-
vascular system, and the neck is the stone-canal. Where this neck
joins the anterior coelom the latter is dilated, and this dilatation is
the rudiment of the axial sinus of the adult.

At about sixteen days the right anterior coelom buds off a solid
mass of cells which, for a short time, remains connected with it by a

xvi ECHINODEKMATA 511

string of cells ; this mass of cells hollows out to form a vesicle, the
madreporic vesicle, but the string of cells vanishes, and the right
coelom never exhibits a dilatation corresponding to that of the axial
sinus on the left side (m.v, Fig. 386).

About the same time the longitudinal ciliated baud becomes
thickened in four places, and bent outwards in the form of four
horizontal semicircular loops. Of these loops two are situated, one
on each side in the re-entrant angle of the ciliated band, between the
antero-lateral and postero-dorsal arms, and these are termed the dorsal
ciliated epaulettes ; and two, one on each side on the course of the
posterior cross-bar, which are termed the ventral ciliated epaulettes.

These four ciliated epaulettes, distinguished as the anterior ciliated
epaulettes, become separated from the rest of the band, which heals
the breaches thus made in its continuity by special growth from the
broken ends (Fig. 386). The four ciliated epaulettes then grow till
they almost if not quite meet each other in the mid-dorsal and mid-
ventral lines ; they form the main locomotor organ of the later larva,
on which they bestow something of the aspect of a tiny medusa;
they are much thicker, and carry much more powerful cilia than the
rest of the band. The aboral ends of all the skeletal rods undergo
resorption

ECHINOPLUTEUS AND OPHIOPLUTEUS LARVAE COMPARED

Leaving aside the ciliated epaulettes, which are by no means
universal in Echinoid larvae, and so far as yet known are confined to
the larvae of the genera Echinus and Strongylocentrotus, we may pass
in rapid review the chief differences between the Echinopluteus and
Ophiopluteus larvae at the height of their respective developments.

The Ophiopluteus has only two calcareous centres for the larval
skeleton, one of which supplies the skeleton for all the larval arms of
one side. The Echinopluteus has five calcareous centres, of which the
two primary supply the antero-lateral and post-oral arms on each
side, the two lateral supply the postero-dorsal arms, and the median
dorsal supplies the two prae-oral arms.

The Ophiopluteus has no prae-oral arms, and possesses a pair of
postero-lateral arms, which are developed first and which are the
main organs of locomotion. The Echinopluteus has prae-oral arms, but
the post-oral arms are developed first, and when postero-lateral arms
are developed (they are absent in the larva of Echinus esculentus,
but appear in the larvae of the Spatangoids) they appear very late,
and are the shortest of all the arms.

It is obvious that the differences so far enumerated are of minor
importance, and would be such as one would expect to find separating
the larvae of two allied families. It is when we come to consider the
metamorphosis of the Echinopluteus larva that the radical differences
between it and the Ophiopluteus become apparent.

512

INVEETEBRATA

CHAP.

METAMORPHOSIS OF THE ECHINOPLUTEUS

The metamorphosis may be said to begin about the fifteenth day,
when the ciliated epaulettes have been formed and the madreporic
vesicle is making its appearance. The hydrocoele has now the form of
a vesicle of a somewhat flattened oval shape when seen in cross-section,
with a wall consisting of a single layer of columnar cells. On the
left side of the larva, between postero-dorsal and post-oral arms, an

IpZ

a.cil.ep

icil.ep

FIG. 387. — Echinopluteus larva of Echinus esculcntus twenty-three days old, viewed from

the dorsal surface. (Original.)

Names as in previous figure. In addition, ji.ci7.ej>, posterior ciliated epaulette.

invagination of the ectoderm can be seen above the spot where the
left hydrocoele is situated. This invagination is termed the amniotic
invagination ; it is lined by cubical cells, which contrast with the
flattened cells of the general ectoderm on the one hand and the highly
columnar cells of the hydrocoele on the other. The amniotic iuvagina-
tion grows inward till its floor becomes flattened against the wall of
the hydrocoele.

As a consequence of the changes which these two adpressed organs

XVI

ECHINODERMATA

513

undergo, the characteristic oral disc of the young sea-urchin is built
up ; and the compound
structure composed of
these two organs is con-
veniently termed the
Echinus rudiment,
though it must never be
forgotten that most of the
body of the larva, and not
merely the Echinus rudi-
ment, is incorporated in
the body of the young sea-
urchin.

The hydrocoele, seen
from the side, appears at
first like a circular disc ;
soon, however, a slight
notch appears in its pos-
terior border, the two ends
of this notch join, and so
the disc becomes a ring.
Before the ring form is

am

FIG. 388. — Diagrammatic trans-
verse sections through the
"Echinus rudiment " of Echino-
plutei larvae of Echinus escu-
lentus ranging in age from
twenty-one to fifty days.

A, Echinus rudiment just
formed by the apposition of the
amniotic cavity and the hydro-
coele. B, hydrocoele a ring ;
amniotic cavity closing. C,
amniotic cavity closed ; primary
tube feet of hydrocoele protrud-
ing into it — epineural folds form-
ing. D, epineural folds united,
covering over epineural cavity —
perihaemal rudiment formed. E,
amniotic roof burst, and primary
tube feet protruding — perihaemal
rudiment developed into dental
sac and radial perihaemal canal,
urn, amniotic invagination and
cavity ; az.t, primary tube foot of
hydrocoelf ; ilent, rudiment of
tooth ; dent.s, dental sac ; ep,
epi neural cavity; e.p.f, epineural
fold ; hi/, hydroeoele ; hy.r,
hydrocoele rin.n ; '•/'•'', Ifft pos-
terior coelom ; p.h, perihaemal
rudiment; /*./(•.;•, perihaemal radial
canal ; >:<:, radial canal of the
water-vascular system.

VOL. I

ax.t

am

r.c

514 INVEETEBEATA CHAP.

complete, therefore, the hydrocoele has the form of a hoop, recalling
its form iu Asterias and in Ophiothrix after metamorphosis has
commenced. The opening of the amniotic invagination becomes
first narrowed and then completely closed, so that it is converted
into a sac with a thick floor which is incorporated with the Echinus
rudiment, and a thin roof which is the amnion.

The subsequent course of the metamorphosis consists mainly in
the enlargement of the Echinus rudiment. The hydrocoele soon
sends out five blunt lobes which protrude as finger-shaped processes
into the amniotic cavity. These are the rudiments of the five radial
water-vascular canals, and of their primary terminal azygous tube
feet (az.t, Fig. 388). In the intervals between them there are formed
five radiating ridges of ectoderm which are termed the epineural
ridges. The crests of these form two diverging lamellae, which
fuse with those of adjacent ridges and so roof in the epineural
canals covering the bases of the tentacles. These epineural canals meet
in a central epineural space, roofed over by a membrane termed
the epineural veil, which forms an upper floor to the amniotic cavity.

From the left posterior coeloin, about the twenty-fourth day, there
are given off five pocket-shaped evaginations situated one under the
origin of each epineural ridge, into the substance of which it projects.
These evaginations are the homologues of the perihaemal pockets of
the Asteroid and Ophiuroid larvae ; they all originate from the left
posterior coelom, while it will be remembered that in the two other
larvae mentioned, one originates from the left anterior and four from
the left posterior coelom. About the same time it can be observed
that the left posterior coelom has sent out right dorsal and right-
ventral horns. They, however, are of small extent in comparison with
the bulk of the vesicle ; they soon meet each other anteriorly and so a
ring is formed, surrounding, not the oesophagus, but the stone-canal.

The Echinus rudiment as thus described forms at first a com-
paratively small, star-shaped organ on the side of the larva, but as
development proceeds it becomes ever larger till it occupies the
whole side of the larva. This consummation is arrived at about the
fortieth day.

The adult central nervous system is formed, of course, from the
ectoderm immediately covering the hydrocoele, and forming the
lower floor of the amniotic cavity. It can be first detected by a
thickening of this ectoderm and a great increase in the nuclei ; this
occurs as early as the twenty-first day. Later, fine fibrils can be
detected at the base of the ectoderm and can be traced into some
of the nuclei.

As the Echinus-rudiment increases iu size, the tube feet become
longer and longer and project farther into the amniotic space.
Pointed spines make their appearance, rising from the upper floor
of the amniotic cavity. There are four spines in each iuterradius
arranged in the form of a lozenge. Each of these spines is a hollow
conical outgrowth of the ectoderm of the upp^r floor of the amniotic

xvi ECHINODEEMATA 515

cavity. It is tilled with mesenchyme cells which have been budded
from the wall of the left posterior coelom. These cells arrange them-
selves in a network, in the interstices of which appears calcareous
matter which consequently assumes the form of a lattice-work — a
negative, so to speak, of the framework of cells to which it owes its
origin. The bases of these spines are thickened so as to look like
collars, and here the contained mesenchyme undergoes transformation
into the muscles which attach the spine to its boss. The overlying
ectoderm develops nervous fibrils.

The perihaemal pockets begin to send off narrow outgrowths
between ectoderm and outgrowth of hydrocoele, and form the two
radial perihaemal canals in each radius, which, in the adult, fuse
into one (p.h.r, Fig. 388). The body of each perihaemal space remains
larger than it does in the Asteroids and Ophiuroids, and on its outer
wall a protrusion appears which projects into its cavity. This pro-
trusion is the formative tissue for one of the teeth, and the body of
the perihaemal pocket into which it projects forms one of the five
dental sacs which, collectively, form the cavities of Aristotle's
lantern.

It is characteristic of the later stages of metamorphosis that the
cavity of the hydrocoele ring becomes enormously distended with
fluid. In the centre of this ring there appears an invagination of
the ectoderm which constitutes the lower floor of the amnion. This
invagination is the adult stomodaeum, a structure which does not
exist in Asteroidea and Ophiuroidea ; a small peg-like outgrowth
protrudes from the stomach towards it, which eventually meets the
adult stomodaeum and the two fuse, and so the adult mouth is formed.

If this description has been followed it will be seen that the
adult mouth is at first shut off from the exterior, not merely by the
roof of the amniotic cavity but also by the epineural veil. The
swelling of the Echinus rudiment has indented the larval stomach ;
it is no longer globular, but hemispherical, a flattened side being
turned towards the Echinus rudiment.

Whilst these changes have been occurring and the Echinus
rudiment has been growing in size, other changes have been occurring
in other parts of the larva. From the tips of the re-entrant angles
of the ciliated band, which are situated between the postero-lateral
and post-oral arms, a pair of ciliated epaulettes become separated
off (p.cil.ep, Figs. 387 and 390). This extra pair may be termed the
posterior ciliated epaulettes. They are characteristic of the larva of
Ecli-inus esculentus ; they do not appear in the larva of E. miliaris.
They make their appearance about the twenty-fifth day.

At the same time three pedicellariae of the ophicephalous type
make their appearance on the larva ; each arises as a little knob-like
outgrowth of the ectoderm, into which meseuchyme cells are budded
from an adjacent area of the coelom. Some of these cells form the
skeleton of the organ and some the muscles. One of these pedicellariae
is situated near the aboral pole of the larva ; this one is not

516

INVERTEBRATA

CHAP.

developed iu the larva of E. miliaris. At the base of this aboral
pediceliaria a plate is developed. The other two pedicellariae are
situated on the right side of the larva, and are supported by a single
plate. A third plate begins to be formed around the madreporic
pore ; this is the beginning of the madreporite. All three plates
belong to the series of basals which we have already encountered in
the Asteroid and Ophiuroid, and which, as shown by Bury (1895),
form the genital plates of the adult. Small spicules, rudiments of
the remaining two plates, can now be detected.

Whilst these changes are occurring, the right and left posterior
coeloms become dilated, approach one another, and fuse at the aboral
pole of the larva ; and from the wall of the left posterior coelom,
where it abuts on the hinder wall of the left anterior coelom, a solid

pro.b

pr.o.b.

pr.oi

FIG. 389. — Diagrammatic side-views of larvae of an Asteroid, Echinoid, and BalanoglossM,
to show the comparability of the apical plate of an Asteroid with the larval brain
of the other two types of larvae.

A, diagram of Bipinnaria larva, viewed from the side. B, diagram of Tornaria larva of Balanoglussid,
viewed from the, side. C, diagram of Echinopluteus larva, viewed from the side, ap, apical plate ; I. In-,
larval brain ; pr.o.li, prae-oral band of cilia ; pr.o.1, prae-oral loop of longitudinal ciliated band.

bud of cells grows out and buries itself in the blastocoele which
intervenes between the stomach and the inner wall of the left
posterior coelom. This is the rudiment of the genital stolon.

About the twenty-fourth day a remarkable larval nervous system
makes its appearance. It arises as a shallow ectodermal pit on the
dorsal aspect of the oral lobe, in the middle line behind the anterior
cross-bar of the longitudinal ciliated band. The ectodermal cells
lining this pit bud off from their bases a thick plexus of ganglion
cells and fibres. The floor of this pit may be termed the apical plate,
and compared with the apical plate of the Tornaria larva (Fig. 389).

As the critical period of metamorphosis approaches, rudiments
of spines make their appearance on the three first -formed basal
plates. These differ from the spines already described, which are
formed from the floor of the arnniotic cavity, in being quadrangular
in section with a crown of diverging points, and in being devoid

XVI

ECHINODEKMATA

517

of the basal collar of muscular and nervous tissue so characteristic
of the adult Echinoid spine.

Other calcareous plates, the terminals, corresponding to the
ocular plates of the adult, are developed 011 the left side of the
larva outside the amniotic cavity.

At a time varying between forty-five and sixty days from the
time of fertilization, metamorphosis occurs, and the larva changes

proa.

sens

muse,
cil.ep

FIG. 390. — Ecbinopluteus larva of Echinus cxi-u/i'/ifus about fifty days old, just about to
metamorphose, viewed from the left side. (Original.)

Letters as in Figs. 3Si> and 3S7. In addition, az.t, azygous tentacle, primary tube lert ; </' i/t.*, dental
sac ; ••)!. /•, epiin'iiral veil, covering the position of the udult mouth ; «/!<*.•, museles of adult spines ; tl.i .
adult nerve ring ; wns, sense-organ at apex of primary lube feet ; './, rudiments of first pair of tube feet.

into a young urchin which we may term an imago. The roof of
the amniotic cavity becomes absorbed in the centre, and the primary
azygous tube feet are protruded. In the centre of the disc of each
there is a sense-organ consisting of a conical prominence of elongated
ectoderm cells. At the base of each a pair of buds may be detected
(t.f, Fig. 390), which are the rudiments of the first pair of tube feet.
The peripheral portions of the amniotic roof shrink back, so that
the terminal plates which they contain come to lie externally to
the tube feet.

518 INVEETEBEATA CHAP.

The larva, rendered heavy by the growth of calcareous matter,
sinks to the bottom, and its tube feet adhere to the substratum.
The larval arms are rapidly absorbed, beginning with the postero-
dorsal on the. left side. The ectodermal covering of these arms
flows back towards their bases; their supporting rods protrude as
naked spines but are soon broken off. The larval stomodaeum
becomes disconnected with the stomach and forms a shallow pit ;
the oral lobe, with the stumps of prae-oral and autero-lateral arms
in which this pit lies, persists for a short time but is soon absorbed.
The larval anus disappears, but the larval intestine persists.

At the same time there is a great increase in the inesenchyme,
which is budded off principally from the left posterior coelom, but
also from the right, and a corresponding diminution in the still fluid
jelly of the blastocoele. The direction right to left in the Echino-
pluteus becomes the direction oral-aboral in the young sea-urchin,
but this axis is greatly diminished in length as the metamorphosis
proceeds, and thus diminution in length must be due to the expulsion
of fluid.

A most remarkable change comes over the staining properties of
the ground-substance of the blastocoele at the time of metamorphosis.
During the whole of the larval period it is exceedingly difficult to
stain, but at the time of metamorphosis that portion of this substance
immediately surrounding the stomach becomes capable of taking up
stain with avidity. This must be due to the exudation of some
proteid substance by the cells of the stomach. This exudation is
the forerunner of an exudation which goes on all through life, and
constitutes this portion of the blastocoele into the blood system of
the adult. It is in reality to be compared with the lymphatic vessels
ensheathiug the human intestine, and, in the adult, the connective
tissue thus modified, instead of forming a continuous mantle round
the stomach, forms a network especially concentrated along two lines
forming the so-called dorsal and ventral vessels.

The imago thus launched on its career is very different from the
fully grown adult. It has at first neither open mouth nor anus,
for the adult mouth, although already formed, is hidden beneath the
epineural veil. The gut forms a simple coil, identical with the
curvature of the larval gut. The five a/ygous tube feet, which
terminate the radial canals, are the only organs of locomotion, and
the canals extend horizontally outwards ; there is no sign of that
meridional course so characteristic of the adult urchin. The slightly
convex dorsal surface is the rudiment of the insignificant adult peri-
proct, but as yet it is greater in extent than the ventral ambulatory
surface. In fact, if the long primary tube feet were supported by out-
growths of the body we should have a young Asteroid before us.

There is little doubt that this post-larval stage represents a former
Asteroid ancestor. The changes which convert this flat discoid
organism into the globular adult are almost of as great importance as
those which convert the Echinopluteus into the urchin ; they take

xvi ECHINODERMATA 519

place very gradually as growth proceeds. The mouth becomes open

B.

FIG. 391. — Oral and aboral views of young sea-urchins immediately after the metamorphosis.

(After von Ubich.)

A, oral view of young imago of EaMnus microtiiberculatus. B, aboral view of voting imago of Xti'uii-
gylocentrdtita liriiln.t. Hj-Bs, the five basal (genital) plates, uh.x/i, aboral spines of imago ; az.t, azygous
(\a imary) tentacle ; ilent, rudiment of tooth ; eji.r, cpiiiruiul veil ; j, rudiment of jaw ; o, position of adult
mouth ; o.s/j, oral spines of imago ; i>eil, pedicellaria ; Tj-Ts, the live terminal (ocular) plates ; t.f, pam-d
tube t'l-ct.

by the shrivelling of the epineural veil, and if the little animal be
kept in salt water which is aerated by forcing air into it, and in

520 INVERTEBRATA CHAP.

which one or more stones covered with the calcareous tubes of Serpulids
are placed, it seems to find food and conditions congenial to it, and it
rapidly grows in size. The paired tube feet enlarge and become
functional ; the oral surface grows more quickly than the aboral one,
and the primary tube feet are thus forced upward. As new pairs of
tuba feet are developed in each radius between the first-formed pair
and the primary azygous one, the latter becomes of less importance,
ceases to grow, and becomes enclosed in grooves in the terminal
plates, which have greatly increased in size.

Alternating with the five terminals are five plates, the so-called
basals, one of which surrounds the water-pore, and which had already
appeared in the late larva. On the ventral surface, in the substance of
the epiueural veil, ten plates appear, two in each interradius. Beneath
each pair the tip of the incipient tooth can be seen (von tlbich,
1913). The teeth probably correspond to the mouth angle plates of
Ophiuroids and Asteroids ; the paired plates, which are the rudiments
of the alveoli or jaws, to the first pair of adauibulacral plates in
the arms of Asteroids and Ophiuroids (j, Fig. 391, A). These corre-
spond to the so-called ambulacral plates of the test of Echinus, which
are external to the nerve cord, not internal to it as are the true
ambulacrals of Asteroidea. The internal position of the first pair
of " adambulacrals," which form the jaws, is correlated with the in-
vagination of the ectoderm round the mouth, in Echinoidea, to form
an adult stomodaeuni.

When once the epineural veil is torn and the mouth becomes
functional, the teeth grow quickly and project externally as long
pointed spines, presenting quite a different appearance to their
retired situation when adult. Numerous spines are added, but these
are all similar to those which were formed from the floor of the
amniotic cavity. The quadrangular immovable spines are confined to
the aboral surface, which is rapidly diminishing in relative size.
New pedicellariae are formed, and especially conspicuous are five
"sphaeridia," one in each radius. These sphaeridia are short-spherical
spines in which the calcareous skeleton is a clear solid mass.

When the little urchin has doubled its diameter the anus is
formed. As the larval intestine has persisted as a blind pouch,
lying in the mesentery, separating left from right posterior coelom
(now oral from aboral), and as the new anus is formed by a growth
of the intestine along this mesentery, it is obvious that the new anus
is formed about where the old one became closed.

The larval stomach is transformed into the first or lower coil of
the adult gut ; the second or recurrent coil is gradually formed by
the increase in length of the larval intestine ; since the mouth and
anus are fixed points, this increase in length can only be relieved
by the bending back of the gut into the second coil (Fig. 392).

The genital rachis and the protecting aboral sinus are formed
just as in Asteroidea and Ophiuroidea. From the rachis five
interradial strands grow out which form the beginnings of the genital

XVI

ECHINODEEMATA

521

organs.

The rudiment of the genital stolon, as we have already
noted, is formed as a bud from the wall of the left posterior coelom,
just as it is formed in Asteroidea. As it grows downwards in the
wall of the axial sinus it becomes more extensive than in Asteroidea,
since it does not merely fill a fold in its wall, but almost completely
surrounds the cavity. The madreporic vesicle also grows downwards

a.stom ^@j

aslom

irit

inl

a a

CL.stom

a stem

FIG. 392. — A series of diagrams showing the changes which the gut undergoes in K<-liinus
esculent us after metamorphosis. The diagrams represent horizontal sections through
the young imago.

A, the condition just after metamorphosis. B, the condition at the time of formation of the adult
anus. C, the beginning of the formation of the recurrent coil of the hit rst inr. D, the condit ion in t hi'
adult, n.a, adult amis ; (i.xt<nn, adult stomodaeum ; int, intestine ; Let, larval anus ; l.xtviii, larval stomu-
daeuin ; in.ji, position of madreporite ; st, stomach.

alongside the axial sinus. As in Asteroidea, the originally single
madreporic pore becomes divided up by folds into the numerous
pores of the adult.

When we compare the life-history just described with the life-
histories of the two Echinoderm types previously described, we see
that the Echinopluteus and Ophiopluteus resemble one another in

522 INVERTEBKATA CHAP.

the absence of a fixed stage, and iu the consequent retention of the
larval locomotor organs till the tube feet become functional. But
the Echinopluteus resembles the Asteroid larva, and differs from the
Ophiuroid larva in forming the adult mouth on the left side. Now
we saw that in all three larvae the larval stoinodaeum shallows out
and disappears, but that in the Ophiuroid, before this happens, the
primary tube feet protrude into the stoinodaeum. We ma}7 thus
interpret the amniotic cavity of the Echinopluteus, into which the
tube feet protrude, as a portion of the stomodaeum which is formed
separately from the rest ; that is, instead of all the stomodaeum being
formed at once and then being twisted to the left, it is formed in two
pieces, one of which persists during larval life and then disappears,
whilst the other shelters the growing tube feet and then shallows
out to form the ectoderm covering the oral surface of the adult.

ECHINOCYAMUS AND MELLITA

The development of Ecliinocyamus jmsillus (Theel, 1892) and of
Mellita testudinata resembles that of Echinus esculentus in all
essential points. The calcareous rods supporting the prae-oral arms
are, however, in the form of a lattice-work, consisting of three parallel
rods connected by cross pieces, and ciliated epaulettes are not formed.

In Mellita, according to Grave (1902), there is constantly present,
in addition to the normal pore-canal, a right pore-canal opening into
the right anterior coelorn, and the two pore-canals unite to open by a
median madreporic pore.

The larva of Echinocardium cordatum, the development of which we
ourselves have studied (1914), develops no ciliated epaulettes, but from
the second day of development a club-shaped aboral spike is developed,
supported by a lattice-work skeleton consisting of three diverging
rods connected by cross pieces. This bears a crest of ciliated
epithelium. The skeleton of this club is based on transverse braces
connecting up the aboral ends of the recurrent and body rods. The
larva also develops horizontally extended postero-lateral arms, which
are supported by branches of the skeleton of the aboral spike, and
also a pair of antero-dorsal arms supported by branches from the
rods supporting the prae-oral arms.

As metamorphosis approaches the aboral spike is absorbed. A
very large number of adult spines are formed before metamorphosis,
and the young urchin presents many points of resemblance to a
regular urchin. Thus the mouth is in the centre of the aboral
surface, and is surrounded by five pointed spines which are very
possibly homologous with the teeth of regular urchins.

EXPERIMENTAL EMBRYOLOGY. ECHINOIDEA

We must now give a brief account of the principal results
obtained by the experiments performed on the eggs of Echinoidea.

xvi ECHINODERMATA 523

These fall into two categories : (1) Experiments on fertilization ; (2)
Experiments with the developing embryo and larva.

1. Seeliger (1804) has proved that if an egg lie broken into
two parts, one of which possesses the nucleus and one of which
does not, both fragments can be fertilized, and both will develop
into apparently normal larvae. Loeb (1910) has proved that if tbe
alkalinity of the sea -water be slightly increased by the addition

of from 1 to 2 per cent of ^ NaHO, it is possible to fertilize the

eggs of some species of Echinoidea with the sperm of Asteroidea,
Ophiuroidea, and Crinoidea. Godlewski (1906) has even fertilized
the enucleated fragments of Echinoid eggs with Crinoid sperm, and
has obtained gastrulae. Finally, Kupelwieser (1909) and Loeb have
succeeded in fertilizing Echinoid eggs with the sperm of Mollusca
(Cklorostoma and Mytilus), and in obtaining larvae which resemble
closely the normal four-armed Echinopluteus.

In some cases, as Kupelwieser has shown (1909), the chromosomes
of the spermatozoon do not enter the first spindle of division which is
formed in the egg ; so that the action of the spermatozoon must be
regarded as stimulating the egg to parthenogenetic development, but
not as conveying its own hereditary qualities ; and in these cases
the resulting larvae show purely maternal characters. But this may
be the case even where a genuine fertilization appears to take place,
and the chromosomes of the spermatozoon enter the first spindle, as
Godlewski showed is the case when the uninjured eggs of Echinoidea
are fertilized with Crinoid sperm.

Still more startling is it to find that this may also be the case, as
Shearer, Fuchs, and De Morgan (1912) have shown, with the hybrids
of Echinus esculentus and E. miliaris, two species which are easily
crossed. Whichever way the hybrid is made it may exhibit purely
maternal characters, and these hybrids have been reared through
the metamorphosis. These authors have also shown that the
character of the hybrid obtained by fertilizing the eggs of Echinus
miliaris with the sperm of Echinus esculentus, varies from year to
year ; in one year it was purely maternal in character, in the next
of a type intermediate in character between the larvae of the two
parent species. Even the hybrid obtained by crossing forms belonging
to different orders of Echinoidea is not always maternal in character,
as we ourselves showed by crossing Echinus esculentus and Echino-
cardium cordatmn. The hybrids between these two species only live
eight days, nevertheless, although the two parents are very widely
separated in systematic position, the hybrids show unmistakable
paternal features as well as maternal ones.

The question now arises whether, if parthenogenetic development
can be initiated in the eggs of Echiuoidea by substances contained in
the sperm of Mollusca, which do not convey any hereditary qualities,
it could not also be initiated by dead solutions of an organic
or inorganic character. This question has been answered in the

524 INVEETEBKATA CHAP.

affirmative. Morgan was the first to discover that the eggs of
Echiuoidea, if treated with hypertonic sea-water, that is, water iii
which the normal proportion of chlorides is increased, will occasion-
ally undergo irregular segmentation and develop into larvae with
feebly developed arms, which lie on the bottom.

Loeb (1910) confirmed this result, but he showed that if the eggs
are first treated with an organic acid, like butyric or valerianic acid,
for a minute or two, they will form a membrane exactly like the
vitelline membrane ; then regular segmentation will commence
and lead to the formation of normal larvae which swim at the
surface. This occurs in but a very small percentage of cases, while
the rest perish by a process of cytolysis whereby the blastomeres
break up into globules. If the eggs, after being treated with the
organic acid, are rinsed in clean sea-water and then transferred to
hypertonic solution, and after a time to clean sea-water, all will
develop into normal larvae. It is to be noted that the time differs
in the case of the eggs of every female examined, and has to be
experimentally determined in each case.

From such experiments Loeb draws the conclusion that the
formation of a vitelline membrane is an important step in normal
development : that this membrane is due to the beginning of a
process of cytolysis initiated by the spermatozoon, since careful
examination shows that the first stage in its development is the
formation of a layer of minute globules which flow together; but
that the spermatozoon also contains a material which checks this
cytolysis when it has gone far enough, and that both these actions
are independent of what may be called the hereditary influence
of the spermatozoon.

2. We now pass to experiments made on embryos and larvae.
Driesch began his investigations (1892) by taking normally
fertilized eggs of sea-urchin, waiting until they had divided into
two or four blastomeres, and then separating them by violent shak-
ing. In this way he was able to show that even one cell of the
S-blastomere stage will produce a perfect larva, so that in this
species the division into cells is not, as Eoux supposed, a division
of the germ into areas destined to form special organs.

He further showed that when one of the first two blastomeres
was separated from the other, the isolated blastomere segmented as if
it still formed half of the egg. Thus a hemispherical cup of cells was
formed, and the edges of this cup were then drawn together by
movements of the cells composing it. In this way a blastula was
formed with half the normal number of cells, which nevertheless
developed into a perfect larva.

He was also able to induce the eight cells of the 8-cell stage
to arrange themselves in one plane, and this was accomplished by
freeing the eggs from their fertilization membrane by means of
shaking them a few minutes after fertilization, and by subjecting
them to pressure. If then the pressure were removed the eight cells

xvi ECHINODEKMATA 525

changed into the 16-cell stage, consisting of two tiers of eight ; this
16-cell stage then became a normal hlastula and subsequently
developed into a normal larva.

It followed that nuclei, which normally would have been situated
at one pole, would now be found at the sides of the larva, and hence he
drew the conclusion that the nuclei are indifferent structures and maybe
exchanged for one another without altering the course of development.

The same result can be obtained by subjecting the developing egg
to a moderate degree of heat, viz. a temperature of about 25° ; the
four lower cells of the normal 8-cell stage will arrange themselves
in one plane with the cells of the upper tier.

When the eggs were freed from their membranes by shaking and
then exposed to water freed from calcium, they segmented normally,
but the segments fell apart. This peculiar effect of sea- water devoid
of calcium has been alluded to in previous chapters. It was first
demonstrated by Herbst (1900). When this happened in the 16-
cell stage, when micromeres, mesomeres, and macromeres had been
differentiated, it was comparatively easy to recognize the fragments,
which usually consisted of from two or four cells, by the size of their
component cells (1900). It was found that such fragments, when
derived from the microrneric pole, generally died, but that when they
developed they grew into perfect larvae ; whereas those from the
anti-micromeric or animal pole, on the other hand, generally lived
and developed into clear, free-swimming blastulae, but could develop
no further.

From this circumstance Driesch drew the conclusion that the
substances which are necessary for the formation of the mesenchyme
and gut are, in the 16-cell stage, chiefly centred at the lower pole
of the egg ; hence when cells from the upper pole are taken they
can never form these organs.

These conclusions were confirmed by cutting the blastulae of
Sphaerechinus in pieces by a pair of fine scissors, as was done with
the gastrulae of Asterias. In early stages the fragments healed up
and formed perfect larvae, but, once the primary mesenchyme was
formed, then fragments from the vegetative half could form gut and
mesenchyme but not the long apical tuft of cilia, while fragments
from the animal half formed the apical tuft of cilia but never could
form gut and mesenchyme.

Sometimes, by the action of the calcium-free water, the two first
blastomeres were incompletely separated ; then there resulted a
flattened blastula which was oval, not circular in section. The long
axis of the ellipse was obviously the line joining the two nearly
separated blastomeres. When the first signs of bilateral symmetry,
which in this case are the calcareous stars, appeared, they were situated
at opposite sides of the short axis of the ellipse. It is thus proved that
the first cleavage furrow is transverse to the median plane of symmetry,
and that in normal development the first two blastomeres produced
from the egg are anterior and posterior, not right and left.

526 INVEETEBEATA CHAP.

When the gastrulae of Spliaerechinus are cut up, even if the
archenteron has already differentiated itself into oesophagus, stomach,
and rectum, if the fragment contains a part of the gut this will
differentiate itself again into oesophagus, stomach, and rectum on a
smaller scale.

This result Driesch holds to be incompatible with any physical
or chemical explanation, but to render necessary the hypothesis of an
indwelling non-material entity — the entelechy, which directs the
material at its disposal to purposeful ends. Driesch will not speak
of organ-forming substances, but of conditions, and he claims that
when the cytoplasm of the egg has been regulated to a certain extent
by the entelechy, in a certain direction, it becomes " stitfer " and
more incapable of " regulation " in a different direction.

But there is the most indubitable evidence that, whether we can
form a mental picture of them or not, such things as onmn-formini>

-1- O O O

substances do exist ; for instance, when the developing tail of a
lizard, after an injury, can be made to give rise to two tails merely
by indenting the growing rudiment, what other explanation can lie
given ? Can the indwelling entelechy be forced to alter its whole
method of action by such an external influence ? Even Driesch's
pons asinorum can be got over, as will be shown below.

When the blastulae of sea-urchins, instead of the segmentary
eggs, are exposed to heat, the gut develops as an external evagination
instead of an invagination. This external appendage can be cut off,
and in this way an anenterous larva is formed. Such a larva can
develop the first four pluteus arms and the stomodaeuni. In this
way it can be proved that the formation of the stomodaeum is in-
dependent of the gut.

Herbst (1893, 1895, 1896) took up the task of testing the action
of different chemicals on the course of the development. He made
solutions of different salts in distilled water, of approximately the same
strength as is constituted by the total salt in sea-water. Small
quantities of these solutions were then added to the sea- water in which
the eggs to be experimented with were placed. He found that the
results obtained depended chiefly on the basic radicle in the salt, and
that they were inversely proportional to the molecular weight of the
salt used ; or, in other words, directly proportional to the number
of molecules. Most of the bases tried produced a larva devoid of
calcareous centres. Such larvae never produced larval arms.

Herbst's most startling result was obtained by the use of the salts
of lithium. To obtain these results the eggs must remain in the
mixture of sea-water and lithium solution from the time they are
fertilized till the blastula stage is reached. If removed sooner the
lithium salt produces the same result as the other salts used, and
eggs submitted to the action of the solution after sixteen cells have
been formed do not yield the typical result now to be described.

If eggs are left in the lithium mixture from the time they are
fertilized until the blastula stage is reached, then they develop into

XVI

ECHINODERMATA

527

motionless larvae which show by their clear protoplasm that they
are healthy. These larvae are divided by a constriction into two
sections, one of which shows by the nature of its cells that it
corresponds to an inverted gut, and the other corresponds to the
ectodermic skin of the gastrula. The effect, then, of the lithium
would be to alter the conditions of pressure in the blastocoele so
that the gut develops outwards and not inwards.

If, as we have seen reason to believe, the process of gut formation
is analy sable into two factors, viz. cell multiplication and inwardly
directed cytotaxis, then the lithium has reversed the direction of the

ect

FIG. 393.— Types of lithium-larva. (After Herbst.)

A, blastula stage of lithium-larva of Sphaerechinus granularis ; ectoderm anil endoderm are not yet
differentiated. B, later stage in the development of the same larva ; the ectoderm carries the long cilia.
C, still later stage in the development of the same, larva ; the ectoderm is beginning to be grooved off
from the endoderm. I>, still later stage; the groove is deep, and the endodermic portion exhibits a
secondary division into a small upper part representing the intestine (?), and a lower part representing
the stomach of a normal larva. E, F, O, lithium-larvae of Sji'"""'''1"'"* yraiiuliiris, in which the lithium
has acted more intensely, in E the ectodermic portion is very small, in F it is reduced to a mere kiml.,
in G it has disappeared, ect, ecUidermic part of larva.

cytotaxis. But that is not all. The longer the eggs lie in the
mixture of sea-water and lithium solution, and the more of the
lithium solution used, the Irigyer is the portion of the larva irli //•//.
corresponds to the ffi.it. This can go so far that practically the
whole of the larva becomes gut, the ectoderm being represented by
a little knob of cells at one end of the vesicle.

Herbst suggests that when the blastula stage is reached the
physiological separation of ectoderm-forming and endoderm-forming
substances is hurried on. He supposes that, in a normal blastula,
the amount of endoderm-forming substance increases as we proceed

528 INVEKTEBKATA

CHAr.

from the animal to the vegetable pole. When the endoderm-forming
substance accumulates, absorptive power is increased and more
lithium is taken in. The effect of this is to increase still further
the amount of endodermic substance and inhibit the formation of
ectoderinic substance, and so more and more of the blastula wall
is transformed into endoderm.

When larvae in which there is still some ectoderm are trans-
ferred to sea-water, they acquire the power of ciliary movement, and
develop an abnormally large number of calcareous spicules which are
arranged in a circle, and a correspondingly large number of arms is
developed ; so that the formation of an arm is dependent on the
stimulus afforded by the presence of a spicule.

We ourselves (1911) have found that in the larvae of both
Echinus miliaris and of Echinus esculentus a right hydrocoele is
occasionally developed. In such cases a right amniotic cavity may
be developed, on the floor of which typical pointed spines may arise.
Further, from the right posterior coelom a series of dental sacs or
perihaemal rudiments may be formed, and finally a second " adult "
oesophagus and mouth. This shows that neither the normal
formation of an amniotic invagination from the ectoderm of the
left side, nor of dental sacs from the left posterior coelom, nor
of an adult oesophagus from the left side of the stomach, is due
to the pre-existence of an invisible rudiment of the structure to be
found in the layer of cells out of which it is formed ; on the con-
trary it is clear all three developmental processes mentioned must be
due to an influence from the hydrocoele acting on the indifferent
sheets of tissue constituted by these layers, i.e. on ectoderm, coelomic
wall, and stomach endoderm respectively. Such influences are termed
formative stimuli.

Hence we may make to ourselves the following provisional
picture of Echinoid development. Very early, before cell division
has occurred, there are constituted in the cytoplasm, by the influence
of the nucleus, definite substances which can cause the formation
of the primary organs. The formation of the substances cannot
be attributed to the daughters of the primary nucleus, because then
it would be impossible to disarrange these daughter nuclei and
yet obtain a typical result.

These substances are at first uniformly distributed throughout
the egg ; as segmentation goes on they become segregated from one
another, and when this segrcg<(tion is complete the formation of the
Ifii/ers, that is, of the primary organs, is Itcgun. When once these
layers are formed they in turn produce substances which act on each
other and cause progressive differentiation. These substances can be
increased or decreased by the action of certain salts. So long as
a fragment of an egg has a certain minimal proportion of an organ-
forming substance, the organ will be formed in typical develop-
ment.

Driesch's pons asinorum regarding the formation of a gut of small

xvi ECHINODEKMATA 529

she, differentiated into its typical regions, out of a fragment of a gut
of larger size, can be surmounted, as Zur Strassen showed, by the
assumption of " formative stimuli " proceeding from the cut ends of
the gut fragment, and determining by their interaction the formation
of constrictions in what was, at first, a uniform tube.

The great difference, then, between the eggs of Echinoidea and
those of Nemertinea, (Jtenophora, Annelida, and Mollusca is that in
the latter eggs the organ-forming substances are separated from one
another at a far earlier date in development ; that, in fact, in these
groups the segmentation of the egg is not merely the multiplication
of nuclei, as it is in Echinoidea, but is already incipient organogeny.

HOLOTIIUROIDEA

Our knowledge of the development of Holothuroidea constitutes
the least satisfactory part of our knowledge of the embryology of
Echinoderinata. A complete series of stages of the external form
is only known in two or three life-histories, viz. those of Synapta
digitata, Synapta vivipara, and Oucumaria planci. In only one of
these cases is a larva formed which leads a free-swimming life for
a considerable time, and which can be compared to the Bipiunaria,
Ophiopluteus, and Echinopluteus larvae which have been described.

The eggs of Cuctimaria planci, and so far as we know of other
species of Cucumaria as well, are yolky, and undergo a shortened
development, in which the larva, although a free-swimming organism,
takes no food but depends for its nourishment on yolk grains stored
in its cells, like the larva of Solaster endeca.

The young of Synapta mmpara undergo the whole of their
development within the body -cavity of the mother, and yet this is
the form which has been most carefully investigated and in which
modern methods have been most conscientiously applied. We owe
our knowledge of the development of tins form to Lyman Clark
(1898), and his results seem to show that in most respects, so far
at least as the formation of internal organs goes, the development of
this form agrees with that of Synapta digitata. This latter we shall
select as type, but we must warn the reader that our knowledge of
its development is very scanty compared to our knowledge of the
development of Asterias rulens, of Opliiothrix fragilis, or of Echinus
esculentus.

SYNAPTA DIGITATA

Our account of the early stages we owe to Selenka, who alone
has artificially fertilized the eggs of this form (1893). Semon has
given a highly defective account of its development and of its
metamorphosis, based on larvae caught in the Plankton, and has
made this account the ground for a most fantastic and improbable
theory of the phylogeny of Echiuoderins (1898). Bury (1889 and
1896) devotes portions of two most valuable papers to the considera-

VOL. i 2 M

530 INVERTEBEATA CHAP.

tiou of the development of Synapta, and corrects many of Sernon's
misstatements. It is the more to be regretted that Synapta has to
be chosen as type, because in its adult anatomy it is one of the most
aberrant members of the class Holothuroidea.

The early development of Holothwria tubulosa has been described
by Selenka (1876) ; this species gives rise to a larva like that of
Synapta., but the adult is one of the least modified of Holothuroidea.
Selenka did not keep his larvae alive more than four or five days.
It is much to be desired that the development of this form should be
studied again. By using pure cultures of Nitscliia as food the
larvae of Cueumaria saxicola have been reared throughout the whole
of their development at Plymouth.

Selenka only found one ripe female Synapta amongst all the
hundreds which were brought to him by the collectors of the Naples
Station. It is probable that this was partly due to the season of year
at which he visited Naples, and partly to the fact that Holothuroids
are not so easily obtained in large numbers as are Asteroids,
Ophiuroids, and Echinoids, at any rate on British shores. Synapta
leads a burrowing life in sand and gravel, and is frequently not
reached by the dredge ; the most hopeful place to find it would be by
search during extreme low tides in sheltered inlets like the Clyde.

The other genera, such as Holothuria, Cueumaria, etc., seem to hide
in crevices amongst stones, and only occasional stragglers are caught by
the dredge. Selenka (1876) secured large numbers of Holothuria by
a contrivance resembling a lobster trap, viz. a box with the lid fastened
down but with a small hole in the top, which he sunk in the sea.

The segmentation of the egg of Synapta, as described by Selenka,
is the most regular as yet observed in the animal kingdom. The egg-
divides into two and then four oval segments, and these divide into
two tiers of four each. At the next cleavage each cell divides by a
radial furrow into two daughters lying side by side ; in this way we
get two tiers of eight cells each.

Already in the 4-cell stage the first trace of the blastocoele
made its appearance as a separation of the blastonieres from
one another in the centre of the egg; in the 32-cell stage,
which consists of four rings of eight cells each, these cells surround
a wide space open above and below (Fig. 394). In the following-
cleavage each cell divides by a longitudinal furrow so that the number
of cells in each tier is doubled. The rings nearest the equator
continue to divide by alternate radial and meridional furrows, but in
the upper and lower tiers some of the cells migrate pole-wards and
form here rings of smaller diameter, so that the open spaces at the
poles are covered in and a closed blastula results.

When 512 cells have been formed, that is at the conclusion of
the ninth cleavage, each develops a cilium and the blastula begins to
rotate within the egg-membrane. The blastula elongates, and a slight
thickening occurs at one pole since the cells in this region become
columnar. This thickening we may regard as a vestigial apical

XVI

ECHINODEBMATA

531

plate (cip, Fig. 395). At the opposite pole the invagination which is
to form the archenteron appears. This is of very small extent in com-
parison with the length of the blastula; it does not, at the period of
its greatest extension, equal in length half the total length of the
embryo.

When the development has reached this point the embryo escapes
from the egg-capsule and begins to lead a free-swimming life. In
Synapta, therefore, the larval life commences with the gastrula stage,
not with the blastula as in the other groups studied.

The mesenchynie is formed only after the gastrula stage has been
reached. It originates, according to Selenka, in two cells given off
from the apex of the archen-
terou which multiply by
division. This is unlikely, it
is more probable that
numerous cells are given off.

\~arch

FIG. 395. — The free-swimming gastrula »t'
Synapta, diyitata. (After Seleuka. )

op, .-qiical thickening; nn-h, uirhenteron ; 1tljit

FK;. 394. —The 32-cell stage in the
segmentation of the egg of Synapta
digitatu- viewed from the side.
(After Selenka )

In;the late origin of the niesenchyme the Sy-nnptu larva resembles the
Asteroid, and the reason for this may be the same in both cases,
namely, the absence of a larval skeleton, to the formation of which
is devoted the primary mesenchynie of Ophiuroids and Echinoids,
which is given off in the blastula stage.

The tip of the archenteron bends at right angles and grows
towards the dorsal side of the larva ; it fuses there with the ectoderm,
and a perforation of the fused layers is effected so that the lumen of
the archenteron communicates with the exterior. This perforation is
the madreporic pore (nip, Fig. 396). After it is formed the horizontal
branch of the archenteron is separated from the vertical one and
becomes the coelom, whilst the vertical section of the archenteron is
the gut. This latter soon becomes divided by constrictions

532

INVERTEBKATA

CHAP.

into oesophagus, stomach, and intestine. Tins last division is
bent forwards, so that, as in other Echinoderm larvae, the alimentary
canal is bent in a curve, concave ventrally. The stomodaeum is
formed in the usual manner on the ventral side of the larva ; it
joins the oesophagus after the coelom has been separated from the
alimentary canal.

The general covering of cilia becomes lost as the ectoderm cells
flatten out, and the cilia become restricted to ridges which form a

slom

cce

FIG. 396. — Two young larvae of Synapta diyitata viewed from the side. (After Selenka. )

A, formation of the coelom. The coelomic part of the archenteron opens to the exterior by the madre-
pnrie pore before it is separated from the gut-portion of the aichenteion. 15, formation of the mouth and
stomodaeum. al, alimentary canal ; up, apical thickening ; hlji, blastopore ; coc, coelomic vesicle ; wf,
madruporic pore; atom, stomodaeum.

folded longitudinal band. This band resembles that of the Bipiunaria
larva of Asteroidea in its earlier stages of development, i.e. it consists
of right and left longitudinal pieces and anterior and posterior cross-
bars, the former of which is bent backwards over the prae-oral region
of the larva as the prae-oral loop, and the latter of which is bent
forwards in front of the anus as the anal loop. An adoral band of
cilia is formed in the same way as has been described for the
Bipinnaria, Ophiopluteus, and Echiuopluteus.

The Holothuroid larva differs from the Bipinnaria in two points :
first, the prae-oral loop, although almost, is never quite constricted
from the rest of the band, so that the longitudinal band of cilia

xvi ECHINODEBMATA 533

remains simple ; and, secondly, the loop-like outgrowths of this baud
remain much shorter than in the Bipinnaria larva. They are usually
called "processes," but as they are homologous with the arms of other
types of Echinoderm larvae we shall call them by the same name.

We find prae-oral arms (pr.o.a, Fig. 398) in front of the mouth
on the side of the prae-oral loop ; at the sides of the anal loop post-
oral arms (p.o.a, Fig. 398); and each side of the longitudinal band
carries an antero-dorsal, an intermediate-dorsal, and a postero-
dorsal arm (a.d.a, int.d.a, piLa, Fig. 398). Where the anal loop
originates from the longitudinal band there is a well-marked postero-
lateral arm. on each side (pl.a, Fig. 398). This arm is the one
which, from a fancied resemblance to the human ear, suggested the
name Auricularia to Johannes Miiller (1850), by which name the
larva is known.

AURICULARIA LARVA

From the foregoing description it is obvious how closely the
Bipinnaria and Auricularia larvae resemble one another in external
appearance, but the Auricularia larva differs widely from the Bipin-
naria in its metamorphosis, and indeed in the internal changes
which precede metamorphosis.

The coelomic vesicle is at first situated in the mid-dorsal line ; it
shifts to the left, and then divides into anterior and posterior portions.
The posterior vesicle divides into right and left posterior coeloms,
which apply themselves to the sides of the larval stomach. This
change has been observed only by Metschnikoff (1869).

The anterior vesicle does not, however, as Selenka and Metschnikoff
imagined, become directly converted into the hydrocoele ; Bury has
shown that it becomes divided into dorsal and ventral parts by a
constriction (1896). The dorsal part, which communicates with the
exterior by the primary madreporic pore, is the left anterior
coelom ; the ventral portion is the rudiment of the hydrocoele,
and the connecting narrow part is the stone canal. Neither right
anterior coelom nor right hydrocoele are developed.

In the Auricularia larva, then, in spite of its outward bilateral
symmetry an inner asymmetry is early evident. The hydrocoele has
the form of a hoop whose plane is the frontal plane of the larva, and
it lies at the left side of the oesophagus. From its outer surface there
arise five lobes, which are not the rudiments of the radial canals of
the water-vascular system, but of the primary buccal tentacles
(11; 2P ov4v 5P Fig. 398). Alternating with these lobes there appear
five much smaller lobes (1, 2, 3, 4, 5, Fig. 398), which are the rudiments
of the radial water-vascular canals.

On these facts Semon's whole hypothesis of the phylogenetic
relationships of the classes of Echinodermata is built. He regards
the first five lobes as equivalent to the five primary lobes of the
hydrocoele in the Bipinnaria, Ophiopluteus, and Echinopluteus larvae,
and therefore equivalent to the radial canals in the Asteroidea,

534

INVEETEBEATA

CHAP.

Ophiuroidea, and Echiuoidea respectively ; tlie radial canals ut' the
Holothuroidea, the rudiments of which are represented by the
secondary lobes of the hydrocoele, would therefore, on this hypothesis,
not be homologous with those of other Echinoderms.

B

coe

ci

il.long

mp

*S\ cillong

a.c

calc

cillong

ac

oes

r.pc

FIG. 397. — Three views of young Anricularia larvae of Xi/intjitit diijitdia viewed from tin'
dorsal surface, showing the division of the coeloni. (After Metsclmikoff. )

A, the coeloni still undivided, but extending far backwards. B, the coelom divided into anterior
and posterior portions. C, the posterior portion of the coelom divided into right and left halves. «.e,
anterior division of the coedoni ; <'</<•, calcareous body ; p. coe, posterior division of the coeloni ; cil.ltniii,
longitudinal ciliated band ; me, undivided coelomic sac ; /./>.<•, left posterior coeloni ; »i/<, ni.-idrporic
port- ; ui'.x-, oesophagus; c.j'.r, right posterior coeloni ; .-•/, stomach; xtnm, stoiiioilai-iiin.

But the whole of this theory is (shattered by our knowledge of the
development of Cucumaria planci, first described by Seleuka but
worked out with care by Ludwig (1891).

XVI

ECHINODEKMATA

535

In this form the first five lobes of the hydrocoele give rise to the
radial canals, and the primary buccal tentacles arise from their bases.
Now in Synapta the radial canals disappear in the adult, they are, in a
word, vestigial functionless structures ; but in Cucumaria they persist
and give rise to numerous paired tube feet. Therefore the mode of
their development in Synapta is secondary, the method in Cucumaria
typical and primary, and this typical and primary method is the
same as that which obtains in other groups of Echinoderms.

calc

Fni. 398. — The fully developed Auricularia larva of Synapta digitafu, viewed from the
ventral surface and from the side. (After Bury. )

A, Auricularia viewed from the ventral surface. The darker regions of the longitudinal ciliated band
indicate the fragments into which it will break at the metamorphosis. B, Auricularia viewed from the
left side. Letters as in previous figure. In addition, I-V, the fragments of the ciliated band which
will give rise to the transverse ciliated bands of the pupa. OR, the fragments of the ciliated baud
which will give rise to the ring surrounding the mouth of the pupa. li-5j, the lobes of the hydrocoele
which will give rise to the lirst tive buccal tentacles. 1-4, lobes of the hydrocoele giving rise to radial
canals, re, anus ; a.e, left anterior coelom ; a.d.a, antero-dorsal arm; c-il.cul, adoral band of cilia; 7i//,
hydrocoele ; int, intestine ; int.d.n, intermediate dorsal arm ; l.nerv, larval nervous system of Semon ;
I'.c. pore-canal ; p.d.a, postero-dors.il arm ; p.l.a, postero-lateral arm ; p.n.n, post-oral arm ; p.o.c, peri-
oral coelom ; I'ir.o.n, prae-oral arm ; st.r, stone-canal.

The mesenchyme in Synapta has by this time formed a- loose
reticulate tissue spanning the blastocoele. In the posters-lateral
process certain of the mesenchyme cells have given -j-ise to typical
calcareous structures which enable us to distinguish the larva of
Si/napta digitata from other kinds of Auricularia (ca/r, Fig. 398, B).
These calcareous bodies are wheels consisting of a central knob,
numerous spokes, and a toothed rim. The knob does not lie in the
same plane as the rim, but beneath it, so that the whole might be
compared to a bowl with perforated sides as well as to a wheel.

536 INVEETEBEATA CHAP.

METAMORPHOSIS OF THE AURICULAlilA

Signs of the metamorphosis now appear. The hydrocoele is still
in the form of a vertical hoop with its concavity directed towards the
right. From the anterior edge of the left posterior coeloni a finger-
like process grows out and extends along the hydrocoele. This is
the peri-oral coelom (p.o.c, Fig. 398), homologous with the peri-oral
coeloin in Asteroidea and Ophiuroidea. At the same time the left
and right posterior coeloms approach each other ventral to the
intestine, and eventually become applied to one another in an oblique
line. The left coelom extends over to the right in front of the right
coelom ; this extension is evidently homologous to the right ventral
horn of the left posterior coelom in the larva of Asterina gibbosa.
Then the longitudinal ciliated baud breaks into fragments, owing, no
doubt, to the fact that the neighbouring ectoderm grows more quickly
than that forming the band.

The following are the pieces into which the band breaks up : — The
prae-oral loop gives rise to a median and two lateral pieces (Fig.
399, A), and the anal loop gives rise to three precisely similar pieces.
Each side of the longitudinal band breaks up iuto four pieces, three
of which roughly correspond to the antero-dorsal, intermediate
dorsal, and postero-dorsal larval arms. The fourth piece corresponds
to the re-entrant angle between intermediate dorsal and postero-dorsal
arms. Finally, each postero-lateral arm gives rise to a separate
fragment of the band.

Semon maintains that even before this stage a larval nervous
system exists (l.nerv, Fig. 398), consisting of two longitudinal ridges
of thickened ciliated ectoderm which are independent of, and within
the field embraced by, the sides of the larval ciliated band. Semon
draws the conclusion that these are nervous, because in sections he
finds that there are fibres at their bases ; but no separate nerve-cells
have ever been discovered. According to Semon, as metamorphosis
proceeds, these bands become carried into the interior of the larva by an
invagination which involves the mouth and form the adult nerve-ring.

Bury gives a different account of the matter, and as Semon has
proved to be inaccurate in other points we follow Bury. This author
points out that by inequality of the rates of growth of neighbouring
parts the mouth is carried over to the left side, and the apical pole
of the larva is displaced to the right. Then a ciliated ring
round the mouth is formed by the juxtaposition of four pieces of the
old longitudinal ciliated band : these four are the median pieces of
the prae-oral and anal loops and the pieces of the sides of the band
mentioned above, which correspond to the re-entrant angles between
intermediate-dorsal and postero-dorsal arms on each side (Fig. 398).

Then the invagination described by Semon occurs, by which the
larval mouth surrounded by the circular ring comes to lie at the
bottom of a deep pit, the aperture of which nearly but not quite
closes ; the opening of this atrium is distinctly on the left side. The

XVI

ECHINODEPJVIATA

537

remaining fragments of the longitudinal ciliated band then join with
each other so as to form five transversely arranged ciliated rings.
Of these the fifth and most posterior is formed by the union of the
fragments formed from the two postero-lateral processes. The next,
i.e. the fourth ciliated ring, is formed by the union of four fragments,
two derived from the remains of the postero-dorsal processes, two from
the lateral fragments of the anal loop. The next, i.e. the third ciliated
ring, arises from the union of the fragments produced by the inter-
mediate dorsal processes.

A B

a

slow

FIG. 399. — Diagrams of the anterior aspect of metamorphosing larvae of Synapta digitata
in order to show the changes undergone by the longitudinal ciliated band. (After Bury.)

A, before metamorphosis into tin- pupa. B, C, during metamorphosis into the pupa. In C the?
mouth has moved to the left. D, after the metamorphosis into the pupa has been almost completely
accomplished. I, fragment which gives rise to the first transverse ciliated band of the pupa. 11",
Ilh, lie, three fragments which give rise to the socond transverse ciliated band of the pupa. Ill",
III'/, two fragments which give rise to the third transverse ciliated band of the pupa. OR, four frag-
ments which give rise to the oral ring of t he pupa. «i>, apical thickening of I he larva ; siom, stomodaeum,
which becomes the atrium ; ?»//, madreporie pore.

The second ciliated ring arises from the union of three fragments,
two baiug the remnants of the antero-dorsal processes, and the third
is the remnant of the right prae-oral process derived from the right
side of the prae-oral loop. The first ciliated ring which immediately
surrounds the opening of the atrium is derived from the left prae-oral
process (Figs. 398, 399, 400).

By the shrinkage of the prae-oral portion of the. larva the opening
of the atrium and the band surrounding it come to be situated at

538

INVERTEBRATA

CHAP.

r

•slom

the anterior pole of the larva, and so the transient asymmetry of the
metamorphosing period is removed, and the larva again attains
perfect symmetry. It is now in the form of a barrel surrounded by
five ciliated hoops, with the atrial opening at the anterior and the
anal opening at the posterior pole, and is known as the barrel-
shaped larva, or as the pupa.

Whilst these external changes have been going on, the hydrocoele
ring has become completed by the union of the two ends of the hoop
which existed in the larva. During the process of the shrinkage of
the prae-oral part of the larva the hydrocoele hoop has rotated till its
plane, instead of being parallel to the length of the alimentary canal,

becomes situated at right angles
to it. Then what was the posterior
and is now the ventral end of the
hoop grows under the oesophagus,
whilst the other end grows over
the oesophagus to the right, bends
down and meets the ventral end
beneath the oesophagus, and so
the ring is closed. Before actual
closure occurs the ventral end can
be seen to grow out into an in-
wardly directed lobe. This is the
rudiment of the Polian vesicle
(Pol, Fig. 401).

The stone-canal opens into the
ring in the interspace between the
first and second of the smaller
Of lobes, that is, between rudiments of
the first and second radial canals,

V-

FIG. 400. — Metamorphosing larva
Synapta digitata viewed from the
ventral aspect. (After Bury.)

counting as first lobe the one most

Letters as in Figs. 398 and 399. In addition, anteriorly Situated, ill the Stage

at, atrium : a portion of tho larval stomodneum ; i , i i n , i i

U, buccal tentacles; cil.tr, transverse hoops where ^6 plane of the hoop IS

of cilia ; r.c, vestigial radial canals. parallel to the long aXlS of the larva.

Therefore the stone-canal opens into

the ring in the same position as in the Asteroidea and Ophiuroidea.
With the closure of the ring the peri-oral coelom also forms a complete
circle, and the ventral horn of the left posterior coelom extends com-
pletely over to the right and round to the dorsal surface, where it
grows towards the main portion of the left posterior coelom, which
we may term its dorsal horn. The two horns are separated only by
the anterior coelom and its extensions, the stone-canal and the pore-
canal, just as is the case in Asteroidea, Ophiuroidea, and Echinoidea.
At the same time the oblique mesentery, separating left posterior
coelom and right posterior coelom, becomes largely broken down, and
this is also what occurs in Asteroidea. The longitudinal mesentery
of the adult is not, as Semon assumed, identical with the space
separating right and left posterior coelomic sacs in the larva, but

xvi ECHINODEEMATA 539

only partly corresponds to this ; it partly represents the space, filled
with gelatinous connective tissue, which separates right and left
horns of the left posterior coelorn. The ciliated ring, which is
invaginated, seerns to give rise to the nerve -ring and to the
ectodermal covering of the first five atrial tentacles, which, as they
increase in length, protrude into the cavity.

According to Lyman Clark (1898), in Synapta vivipara the mouth
comes to protrude from the floor of the atrium as a papilla. This
papilla grows upwards, and its margin fuses with the sides of the
atrial cavity high up ; and in this way a portion of the atrial cavity
becomes completely enclosed in the form of a ring surrounding the
mouth. This ring is the epineural canal, which overlies the ring
nerve. There is no doubt that a similar process takes place in
Synapta digitata. At the same time the rudiments of the radial
canals (r.c, Fig. 400) grow out and bend backwards, and extend along
the radii. In Synapta vivipara, according to Clark, the rudiments
of the radial canals remain entirely vestigial, and never grow back
along the radii.

The pupa swims about for a considerable time, and is only very
gradually transformed into the adult. As the tentacles grow in
length the atrial opening is widened, and they protrude freely to
the exterior and develop their lateral branches. At this stage the
pupa, as figured by Metschnikoff (1869), seems to have only four
transverse hoops of cilia, so that one of the five must have dis-
appeared. The intestine, which until now has projected straight
backwards, develops a knee-like bend where it issues from the
stomach, and the loop formed by this hinge grows forward till it
nearly reaches the level of the hydrocoele. In this way the ascend-
ing and descending limbs of the intestine are formed.

The peculiar otocysts (ot, Fig. 401) which distinguish Synapta
are developed as evaginations of the epineural canal. The ring of
calcareous ossicles surrounding the oesophagus is developed from
mesenchyme cells which come to lie between the oesophagus and
the nerve-ring. By these cells first five radial pieces, and much
later five interradial pieces, are formed. An accumulation of
mesenchyme cells also clusters round the anterior coelom, and
here forms the calcifications which are known as the secondary
or internal madreporite. Thus the remnant of the anterior
body-cavity is enclosed, and it becomes pierced by pores which
communicate with the coelom and which are lined with ciliated
epithelium. The primary pore-canal and the pore disappear.

Soon after the atrium has opened out and the tentacles have
become protruded, the transverse ciliated bands disappear, and the
pupa sinks to the bottom and takes up the life of the adult. The
stage with five tentacles is called by Semon the Pentacula stage.

The development of the genital organs has been observed by
Clark in Synapta vivipara. In this species the eggs, when ripe,
burst the covering of the ovarian tube and fall into( the body-cavity

540

INVERTEBEATA

CHAT.

of the mother, and here they are fertilized. They develop very
rapidly ; the segmentation of the egg and formation of the layers is
exactly like what it is in Synapta digitata. The embryo, however,
never develops either the folded ciliated band of the Auricularia or
the transverse bands of the pupa ; it is an oval organism uniformly
ciliated all over. The stomodaeuin arises on the ventral side, and
becomes displaced to the left and then to the anterior pole. The
larval anus disappears early, and the anus is re-formed later in
development. The genital organ arises as a thickening of the

cQ.tr

B

•mp

Pol

calc

calc

caTc

FIG. 401. — Pupa of Rynapta diyitata in two stages of development. (After Metsclmikoff. )

A, before the bnccal tentacles have been protruded from the atrium ; note the five transverse ciliated
bands. B, after the buccal tentacles have been protruded from the atrium ; note the four transverse
ciliated bands. Letters as in previous figure and in Fig. 398. In addition, at, atrium, i.e. larval
stomodaeum; i-nlr.h, rudiment of buccal skeleton ; ot, rudiment of otocyst ; 1'vl, rudiment of Folian
vesicle ; at.c, stone-canal.

epithelium covering the right hand side of the mesentery carrying
the stone-canal, i.e. from where the right horn of the lift posterior
coelom impinges on the anterior coelom.; the enlarged cells burrow
into the gelatinous substances of the mesentery, there form a
spherical mass which grows out into the genital tubes, and later
forms its own duct leading to the exterior.

Beyond all doubt the process of the development of the genital
organs is the same in X//tirtj>/<t di<ji/at<t. Stages in the development
of the genital organs of Cucumaria glacialis have been observed by
Mortenseu, who confirms Clark's account (190 -t). The spot where
the genital cells make their appearance is therefore the same in

xvi ECHINODERMATA 541

Holotlmroids as in Asteroids, Ophiuroids, and Echinoids. The
Pentacula stage is soon passed, since accessory tentacles arise just
over the spots where the radial canals are formed in Synaptct digitata,
and, in S. vivipara, from the rudiments of these canals. Thus we
have a ten-tentacled stage, and the full adult condition is attained
by the development of accessory tentacles in the dorsal interradii.

OTHER HOLOTHUROIDS

The only other of the species whose development exhibits an
Auricularia larva, about whose life -history anything is known, is
•Hblothuria tubulosa. For this we are indebted to Seleuka (1876),
who secured great numbers of adult individuals, and had the luck
to obtain a ripe male and female which spawned spontaneously, and
in this way a natural fertilization was obtained. The egg segments
with great regularity, and gives rise to a spherical blastula of about
200 cells, which acquire cilia ; the embryo then escapes from the
egg-membrane and becomes a larva in the blastula stage, as in
Asteroidea, Ophiuroidea, and Echinoidea — not, as in Synapta, in the
gastrula stage. Then one side of the blastula becomes thicker than
the rest, and becomes flattened. On this flattened surface the
archenteric invagiuatiou appears, and from its apex, even when
slightly developed, copious mesenchyme cells are given off.

The archenterou only projects a short distance into the blastocoele,
so that there is a large prae-oral section of the larva. From the
apex of the archenteron a large coeloinic vesicle is given off, and the
longitudinal ciliated band becomes established in the usual way, and
then, afterwards, a vertical outgrowth is developed which forms the
pore-canal ; so that in this respect also Holothuria agrees with other
Echinoderms and differs from Synapta, in which the pore-canal
and madreporic pore are formed before the coelom has separated
from the archenteron. The stomodaeum appears on the ventral
surface as usual, and so the gut is completed, but the intestine
bends forward as it does in other Echiuoderm larvae. The
coelomic vesicle divides into anterior and posterior portions, and
the latter divides into right and left halves, just as in Synapta.
The hydrocoele develops five lobes, but beyond this stage Selenka
could not rear the larvae — a fact much to be regretted, as the
development, so far as it goes, shows signs of conforming in every
way more closely to the type exhibited by other Echiiioderm larvae
than does that of Synapta.

The development of Cucumaria planci has also been worked out,
so far as external features are concerned, by Selenka (1876), and his
account, in which there are many errors, has been corrected by
Ludwig (1891). The eggs were obtained by spontaneous spawning,
and a natural fertilization resulted. The segmentation is regular
and results in the formation of a regular spherical blastula, although
the eggs contain much yolk. Development is complete in about

542 INVERTEBRATA CHAP.

twelve days, but an Auricularia larval stage is never developed, and
the larva in its earty stages takes no food. The mesenchyme
appears to be formed in the blastula stage, as in Echiuoidea and
Ophiuroidea, from one side of the blastula wall; it is this area
which is later invaginated to form the archenteron. The coelom is
separated off and divides exactly as it does in Holothuria and
Synapta. Then the stoinodaeum is formed, and the cilia are reduced
so as to form five transverse rings. Were it not that a prae-oral
region is retained which is covered with cilia, also an anal field in
the neighbourhood of the anus, we might compare the larva to the
pupa of Synapta.

Ludwig was able to determine that the covering of the buccal
tentacles, and also the nerve-ring which connected their bases, took
their origin from the ectoderm lining the larval stouiodaeum. The
tentacles arise from the radial canals and protrude into an atrium
which is the larval stoniodaeum. These radial canals are the first
and only lobes developed from the hydrocoele ring. As the prae-oral
lobe diminishes the mouth is gradually shifted to the anterior pole, and
the cilia disappear. The paired tube feet appear on the radial canals,
first on the mid-ventral one, and then, much later, on the lateral
canals, and lastly on the dorsal one (Fig. 402). Unpaired tube feet
seem not to be developed, i.e. the tips of the radial canals do not
protrude as azygous tentacles. The ectoderm covering the tube
feet is developed as nervous discs before the outgrowths from the
radial canals appear. As soon as the first tube feet have developed
the young Cucumaria sinks to the bottom and begins its creeping life.

An examination of young imago-stages of Cucumaria, just after
the metamorphosis is complete, yields many most interesting results.
Ludwig was able to keep the young Cucumaria planci alive for
four months, and we ourselves have examined a series of young
Cucumaria from the Antarctic (1912). The pore-canal is lost, but
there is an anterior coelom embedded in the body-wall in which the
stone-canal ends. This anterior coelom was seen by Ludwig, who,
however, regarded it as a secondary evagination of the stone-canal.
The walls of the atrium, i.e. the larval stouiodaeum, have split into
five valves (v, Fig. 402), and each valve is supported by a calcareous
plate. A perfect cuirass of overlapping calcareous plates is found
everywhere in the skin. The alimentary canal is still straight,
but as the animal grows older the intestine lengthens and becomes
thrown into a forwardly directed loop, and ciliated pores appear
connecting the anterior coelom with the body-cavity, and in this way
the secondary or internal madreporite is formed.

On reviewing the comparatively disconnected series of facts
which we have just considered, it is clear that the larva of
Holothuroidea, in spite of its external similarity to the Bipinnaria, is
profoundly dissimilar when its internal anatomy conies to be con-
sidered. Thus, though both types of larvae possess a prae-oral lobe,
that of Bipiunaria contains extensions of the left and right coelomic

XVI

ECHINODEKMATA

543

sacs, wliilst that of Auricularia is. filled with inesenchyme. The
mode of segmentation of the coeloni is widely different in Auricularia
from what it is in Bipiunaria. Ou the other hand, the retention of
the larval mouth and its shift towards the left, as seen in Holo-
thuroidea, is not found in Asteroidea or Echinoidea, and is paralleled
only hy the development of the Ophiuroidea.

The growth of the buccal tentacles into the atrium, i.e. the larval
stomodaeum, recalls what occurs in Ophiuroidea and in Echinoidea,
if our conception of the amniotic space of the latter as a separated

v

cole

calc

FIG. 402. — Post-larval stage in the development of Cucumaria x<u'i<:f>l<i viewed

from the side. (Original.)

b.t, buccal tentacles ; (./, paired tube feet ; t; valves into which the atrium splits.

portion of the stomodaeum be admitted ; hut there is an important
difference, for the primary tentacles of Asteroidea, Ophiuroidea, and
Echinoidea are the tips of the radial canals, but the tips of the radial
canals of Holothuroidea do not protrude into the atrium, only their
basal branches, the buccal tentacles, do so. More light on this interest-
ing difference will be obtained when the complete history of Cucumaria
saxicola is worked out. This species, which is very closely allied
to Cucumaria planci, has been reared through the metamorphosis
by the authorities of the Plymouth Biological Station.

The adult anatomy of a Holothuroid suggests the view that the
group may have been derived from early Echiuoidea in which the test

544 INVERTEBBATA CHAP.

consisted of plates movable on one another. This view is strengthened
by the complete armour of plates in which the young Cucumaria is
enveloped, and which gradually become separated from one another as
the animal grows older, owing to the more rapid growth of the inter-
stitial tissue ; the manner in which the intestine grows after meta-
morphosis is complete also resembles what occurs in the Echiuoid.

But if Echinoidea and Holothuroidea have diverged from a
common stock, then the Echinoid larva has been much modified
since that time in its external appearance ; whilst in the Holothuroid
larva the internal asymmetry in the development of the coelom has
been pushed back to a very early period of development.

CRINOIDEA

The group of the Crinoidea is perhaps the most interesting-
division of Echinoderniata because it is the dying remnant of the
class Pelrnatozoa, a class which once was represented by an enormous
number of forms, and by such crowds of individuals that their
skeletons form mountains of limestone in certain localities.

The development of only a single species, viz. Antedon rosacea, is
known, and this species has yolky eggs, which only develop into a free
swimming larva on the fifth day. This larva has a very brief free
life, during which the mouth does not communicate with the stomach,
and, consequently, no food is taken in. We cannot, therefore,
compare this larva directly with such larvae as the Bipinnaria,
Ophiopluteus, Echinopluteus, and Auricularia, but rather with the
larva which emerges from such yolky eggs as those of Solaster and
Cribrella.

Although Antedon rosacea is confined to the Western Atlantic
and to the Mediterranean, other species of Antedon occur all over the
world, and there is no reason to think that the development of any
of these differs in any important respect from that of Antedon rosace a.

Leaving aside the earlier authors, such as Carpenter (1866), who
described the external features of the development, we find that we
have only to take account of the work of Bury (1888) and of Seeliger
(1892), who investigated the development by means of modern
methods. These two workers used practically the same methods, and
their results happily confirm one another in all but unimportant
details. Perrier (1880) deals, strictly speaking, with the post-larval
development. As his work is earlier than that of Bury and Seeliger,
and as, moreover, his methods are not so perfect and his starting
point is later, it is quite obvious that he has not been so successful
in unravelling the complex relations of the organs in the just meta-
morphosed larva, as they have been. To Bury belongs the credit of
being the first to determine with accuracy the real course of Crinoid
development. Seeliger, who came after him, did little but confirm his
results. Both Bury and Seeliger obtained their material by the
natural fertilization of the eggs.

xvi ECHINODEEMATA 545

Antedon, unlike Holothuroidea, lives in the open and can usually
be obtained, when it is found at all, in enormous numbers by means of
the dredge. At proper seasons of the year, ranging from May in the
Mediterranean to July in the Clyde, a few ripe males and females are
certain to be included in the haul. These, when placed in clean
sea-water in the aquarium, will emit sperm and eggs early in the
morning, about 7 A.M.

Both Bury and Seeliger found the best preservative to be a
concentrated solution of corrosive sublimate in sea-water, to which a
small proportion (Bury used £, Seeliger ^V) °f glacial acetic acid has
been added. For the study of the development of the calcareous
plates the embryos must be preserved in spirit alone.

The fertilized eggs adhere to the under side of the pinnules of
the parent by means of a glutinous egg-membrane, and from these
eggs free-swimming larvae emerge on the fifth day.

The fertilized egg divides into two and then into four equal seg-
ments; in the 8 -cell stage, however, the four blastonieres at the
animal are smaller than the four at the vegetative pole. The blasto-
coele appears as a narrow central separation of the blastonieres in
the 4-cell stage, which in the 8- and 16-cell stages is wider at the
vegetative end. In the 32-cell stage it becomes closed at the animal
end by the displacement of the blastomeres ; in this stage the vegeta-
tive pole is surrounded by eight specially large blastomeres. In
the 48 -cell stage these eight blastomeres approach one another and
close the opening at the vegetative pole. These eight blastomeres,
however, subsequently divide, so that when 128 cells are formed and
the complete blastula stage is attained no difference in the size of
its component cells can be detected.

The blastula stage is attained in about eight hours. Then it
becomes converted into a gastrula by the appearance of a pit on its
surface and the invagination of a portion of its wall to form the
lining of the archenteron. This pit or blastopore is not circular in
outline but slit-like, and the long axis of this slit is at right angles to
the plane of symmetry of the gastrula, which is no longer quite
spherical but slightly elongated in one direction. The slit becomes
crescentic, with the horns curved backward, but the archenteron is
curved forward.

As soon as the archenteron is partly formed numerous mesenchyme
cells are given off from its free apex and wander into the blastocoele.
These cells arise in two ways ; either a cell in the wall of the
archenteron buds off a mesenchyme cell, or else it escapes bodily from
between its neighbours in the archenteric wall. As the iuvagiuation
proceeds the blastopore becomes reduced in size till it forms a small
pore, and finally, when development has gone on for thirty-six
hours, it is closed, although a groove marks for some time the spot
where it existed.

The archenteron is flattened in the plane of the blastopore, i.e.
in the transverse plane. In the second night, i.e. in about forty
VOL. i 2 N

546

INVERTEBRATA

CHAP.

hours, it becomes constricted by a ring-like groove into an anterior
and a posterior vesicle (Fig. 403, B). The latter becomes very much
extended transversely, and narrowed in the middle, where it is
embraced by two horns of the anterior vesicle, a dorsal and a
ventral one, which grow backwards and surround the middle portion
of the posterior vesicle like a ring.

acoe

Fia. 403. —Early stages in the embryonic development of .1 ntcdoii rtinacm. (After Seeliger. )

A, sagittal section through an embryo twenty-six hours old in the gastrula stage. B, longitudinal
frontal section through an embryo forty-eight hours old, to show the division of the archenteron into
two coelomic vesicles. C, longitudinal frontal section through an embryo fifty-seven hours old, to show
the belated formation of the alimentary canal. I), longitudinal sagittal section through an embryo
seventy-five hours old, to show the complete division of the coelom and the formation of the hydrocoele.
a.c, anterior coelom ; a.coe, anterior primary division of the coelom ; a.l, rudiment of alimentary canal ;
arch, archenteron ; in/, hydrocoele; /.y/.r, left posterior coelom; mes, mesenchvme ; y-.r<>c, posterior
primary division of the coelom ; r.yi.c, right posterior coelom.

During the third day the embryo, which is now oval since it has
grown more quickly along one diameter than the other, acquires a series
of transverse ciliated rings which at first sight remind us of those of
the Holothurian pupa, for there are five of them formed, and in
addition an apical tuft of long cilia termed the apical field. The first
of the five rings surrounds this field but is incomplete ventrally ; the
rest, however, are complete. The ectoderm cells constituting these

xvi ECHINODEKMATA 547

rings are in active division. Some of the cells constituting the apical
field lose their cilia and retreat to the bases of their neighbours, and
here form ganglion cells ; in this way an apical plate comparable to
the apical plate of the Trochophore larva is formed, from whence a
cord of nerve fibres extends down on each side of the ventral surface
of the larva.

Whilst these changes are going on the anterior vesicle of the
archenteron becomes constricted into a narrow, elongated dorsal
portion and a spherical ventral portion. The former is the rudiment
of the anterior coelom, the latter of the hydrocoele.

During the fourth day the dorsal and ventral horns, which grew
back from the anterior vesicle, unite and form the gut, which thus
at first has the form of a ring surrounding the narrow middle part of
the dumb-bell-shaped posterior vesicle. The narrow part of the dumb-
bell becomes a solid cord of cells and then disappears, and the ring-
shaped gut becomes a sac by the filling up of the cavity of the ring.
The right and left halves of the posterior vesicle become the
right and left posterior coeloms respectively. These shift slightly
one from another so that the right extends slightly on to the dorsal
side of the embryo, the left on the ventral surface.

The anterior coelom, just after it separates from the hydrocoele,
sends out on the right side a small outgrowth. This is probably the
rudiment of a right hydrocoele. The anterior coelom becomes
completely constricted off from the hydrocoele, and both are divided
from the definitive gut. The primary madreporic pore is formed
by an outgrowth from the hinder end of the anterior coelom meeting
the ectoderm on the left near the ventral line.

The larval stomodaeum then appears as a thick -walled in-
vagination on the ventral surface of the larva between the second and
third ciliated rings, which it presses apart. It is therefore evident
that these ciliated rings are not strictly comparable with either those
of the Ciwumari((. larva or the pupa of Synapta. The two cords of
fibres proceeding from the apical nervous system pass down its sides.
Behind the apical field and in the gap of the first ciliated band is a
small glandular pit in the ectoderm. This is the fixation pit, by
which the larva eventually attaches itself to the substratum. The
floor of the stomodaeum does not come into contact with the wall of
the gut, so that the larval alimentary canal, which is devoid of an
anus since the blastopore became closed, does not acquire a mouth,
but it does come into close contact with the hydrocoele which is
flattened against it.

During the fifth day the embryo escapes from the egg-membrane
as an oval larva and swims about by means of its ciliated bands.
This phase of its development may last from a few hours to four or
five days. About this time the calcareous ossicles can be made out,
embedded in the mesenchyme. Of these we have two oblique rings
of five ossicles encircling the hinder part of the body — the hinder
ring is known as the oral ring of plates, the front one as the basal

548

INVEKTEBKATA

CHAP.

ring1 of plates. In front of the latter are a group of three very
small under-basal plates, whilst in front of these there is a linear
series of eleven columnals, each a crescent-shaped ossicle with the
concavity directed ventrally.

At the conclusion of free-swimming life the larva fixes itself by its
adhesive pit to the substratum, and its anterior portion, surrounded
by the columnals, becomes converted into the stalk of the young
Crinoid; but if the free-swimming life lasts longer than one day
considerable readjustment of the internal organs takes place before
fixation occurs.

The shift of the right and left posterior coeloms on each other

B

sfom

FIG. 404. — External views of the embryo and larva of Antcdon rosacca, showing the
mutual relations of stomodaeum and ciliated bands. (After Seeliger. )

A, embryo just before hatching, ventral view. B, larva one day after hatching. Letters as in
previous figure. In addition, ap, apical plate ; cll.tr, transverse bands of cilia ; Ji.i; fixing disc ; stum,
larval stomodaeum — the rudiment of the future vestibule.

increases till the right has become almost completely dorsal and the
left ventral, but the latter does not extend ventrally between hydrocoele
and ectoderm. In addition to this dorso-ventral shift, a shift in an
antero-posterior direction takes place, so that the left coelom shifts
posteriorly until it covers the posterior end of the gut, whilst the
rif tit coelom shifts anteriorly. If we disregard this second shift and

O " ^ ,

consider the relative positions of the right and left posterior coeloms,
when they have just separated from one another, as marking the right
and left sides of the embryo, then we should say that the hydrocoele,
instead of being mid-ventral, is well up on the left side, and so is the
primary madreporic pore ; the larval stomodaeum will also then be
an organ of the left side. When the second, the antero-posterior
shift takes place, if the description given above has been followed, it

XVI

ECHINODEKMATA

549

will be seen that the longitudinal mesentery separating the left and
right posterior coeloms runs in a curve, the concavity of which is
directed forwards.

During free-swimming life the hydrocoele, which lies in a concavity
of the gut, takes on a hoop-like form with the concavity directed
towards the left ; later it rotates so that the concavity is directed
forwards, and it is then seen that the right limb is thicker than the
left. The five primary lobes, the rudiments of the future radial

col

Fie. 405. — External views of larvae of Antedon rosacea — at the time of hatching arid
after fixation, in order to show the development of the calcareous ossicles. (After Seeliger.)

A. larva at the time, of hatching. B, larva two days after hatching — fixed. Letters as in previous
figure. In addition, col, rudiments of the columnal plates ; B'-B5, rudiments of the five basal plates :
f.f, foot-plate ; O!-O5, rudiments of the five oral plates ; SB, rudiments of the under-basal plates.

canals, arise as ventrally directed outgrowths. The stomodaeum
closes behind so that its opening becomes narrowed. The right
posterior coelom sends forward two dorsal diverticula which lie above
the anterior coelom. These two fuse with one another ventrally, but
their lateral walls, where they are in contact with one another, form
the longitudinal mesentery of the right coelom. From their apices
spring five narrow diverticula whose openings are arranged in a circle;
these extend forwards to the apical field and constitute the rudiment
of the chambered organ (Fig. 406, B). The left coelom extends so far

550

INVERTEBRATA

CHAP.

over to the right posteriorly, that it becomes horse-shoe shaped with
the concavity of the horse-shoe directed forwards.

If the free -swimming stage lasts long the rudiment of the
oesophagus appears as a solid peg-like outgrowth of the stomach,
which grows between the two limbs of the hydrocoele towards the
floor of the stomodaeum ; and the rudiment of the stone-canal also
appears as an outgrowth from one end of the hoop-shaped hydrocoele.
According to Seeliger the original connection between anterior coelom

Stx

al

FIG. 406. — Longitudinal sections through free-swimming larvae of Antedon rosacea.

(After Seeliger.)

A, section in the sagittal direction, but not in tin1 sagittal plane, through a larva which has just
been hatched. B, median sagittal section through a larva which lias been hatched for twenty-Hghl
hours and is about to fix itself. Letters as in two previous figures. In addition, ax.c, one of the axial
prolongations of the right posterior coelom ; c/i.o, rudiments of the chambered organ — outgrowths of the
right posterior coelom ; l.neri', fibres of the larval nervous system.

and hydrocoele was in the middle of the hoop, as in Opliiura brevis,
and for that matter in Asterina gibbosa also. The mesenchyme in
the anterior portion of the larva, towards the centre, consists of
closely packed rounded cells, and in these the calcareous columnals
are formed, but towards the periphery the mesenchyme forms
elongated fibre-like cells, which later form muscles and fibres in the
stalk of the young Crinoid. Each lobe of the hydrocoele develops a
pair of lateral lobes, and the original five lobes begin to protrude into
the stomodaeum as free tentacles (Fig. 405, B).

Then the larva, having found a suitable spot, fixes itself to the

XVI

ECHINODERMATA

551

substratum by the secretion of the prae-oral pit. At first it lies
with its length parallel to the substratum, but it soon becomes
erected so as to stand at right angles to the substratum. The stomo-
daeum becomes completely closed from the exterior, and so resembles
the aniniotic space of the Echinopluteus
larva ; it rotates backwards along the
ventral surface till it comes to occupy
the posterior pole of the larva, the body
of which becomes differentiated into a
narrow anterior portion, the stalk, and
a posterior broader part, the cup or
calyx. This calyx becomes pentagonal
in section, and so the radii of the
Crinoid are marked out, and the lobes
of the hydrocoele soon come to corre-
spond with the sides of the pentagon.

The fixation pit flattens out to
form a fixing disc, which becomes sup-
ported by a calcareous foot-plate. The
cilia are shed, and the cells which
formed the ciliated bauds secrete a
cuticle and then retreat from the surface
to some extent, touching it only by
thin prolongations ; processes from the
mesenchyme cells extend up between
them and it soon becomes absolutely
impossible to discriminate between
ectoderm and mesenchyme. The same
fate befalls the ectoderm cells forming
the intermediate areas, indeed it some-
times happens to them before fixation.
The ectoderm lining the stomodaeum,

which has now become the closed FK)- 407.-Fixed larva of
vestibule, however, undergoes none of
these changes. Where it covers the

sacc

Ipc

mtl
'torn

az.t

•osacea, three and a half days after
hatching, viewed from the side —
decalcified. (After Seeligcr. )

and the tentacles it is a -M, axial 01 -an containing the -enital

thick SyilCytium, elsewhere it is a thin stolon; as./, axial band of fibres surround-

1 f 41 "if i n '"K the chambered ornan ; az.t, azy-mis

layer Ot flattened CellS. primary tentacle or the hyilrocoele ; int.

The number of tentacles becomes rudiment or the intestine; int.t, inter-
raised to twenty-five by the appearance ™dial tentacles; oes_ oesophagus; pt

. J •' t r _ paired tentacles; »</r, rudiment ot sac-

ot another pair in each radius, situated c,,ius; r.p.c, n.-ht posterior coeiom; st,
below those already formed and ap- stomach; stom, lan-ai stomodaeum now

;i • i • ,1 o j i become the vestibule.

parently springing directly from the

hydrocoele. The first pair of tentacles also come to spring directly
from the hydrocoele ring, by the absorption into this ring of the base
of the primary tentacle of which they were outgrowths. All these
tentacles become long and protrude into the vestibule, but the last
formed are shorter and not so extensile as the first formed. All the

552 INVERTEBKATA CHAP.

tentacles which belong to one interradius are connected by a
common web of ectoderm.

The gut swells out into a globular form ; wandering cells are
budded from its wall, pass into its cavity and are absorbed. From
its right side a small horizontally directed pouch grows out. This is
the rudiment of the intestine which now grows from right to left,
lying in the septum dividing the left from the right posterior coeloni.
The left posterior coelom has been carried back along with the
stomodaeuni or vestibule, and has now become thoroughly posterior
or oral in position, whilst the right posterior coeloni is now quite
aboral. The main body of the left posterior coeloni wedges itself in
between stomach and hydrocoele, and it is henceforward known as the
oral coelom. Between its two limbs lies the oesophagus. Its right
limb also extends inwards beneath the gut so that the opening of the
horse-shoe, instead of being directed forwards, is deflected to the left.
The left horn of the right posterior coelom wedges itself in between
the left posterior coeloni and the gut, and here fuses with the right
ventral horn of the left coelom, and the two cavities merge in one
another. The right posterior coelom is now termed the aboral coelom.

On the right side the main "body of the right coelom covers the
left internally. The two partially coalesced anterior diverticula of
the right coelom, by whose opposition the vertical mesentery is
formed, extend away forwards and form a central canal surrounded
by the five rudiments of the chambered organ. The walls of these
rudiments have become thinner and their cavities swollen, especially
at their bases, and so the ampullae of the chambered organ are formed.
The anterior extension of the anterior coeloni has disappeared, and
this space becomes reduced to a small rounded sac on the ventral side,
opening by the primary madreporic pore (p.c, Fig. 405, B).

The rudiment of the genital organs appears as the so-called axial
organ, which is equivalent, although not exactly homologous, to the
genital stolon of other Echinoderms. It appears as a line of
enlarged cells on the left side of the longitudinal septum of the right
coelom. In the groups so far studied it seems to arise as a prolifera-
tion of the wall of the left posterior coelom. This line or cord,
becoming detached from the epithelium of the coelornic cavity, sinks
into the gelatinous substance of the mesentery and then grows
backwards, i.e. towards the calyx or cup ; the hinder portion is in the
condition of a thickening of the epithelium, whilst the front part is
already sunk inwards.

The calcareous plates, i.e. the orals and basals, which in the
free-swimming larva formed oblique circles round the body, now form
transverse circles ; the orals surrounding the vestibule, the basals the
aboral coelom. Five sacculi (Fig. 407) are formed in the wall of the
vestibule alternating with the orals. These sacculi are clumps of
uieseuchyme cells which become hollowed out and secrete a bright
yellow pigment ; they are probably of an excretory nature.

Next, the oral vestibule becomes opened to the exterior, the

553

xvi ECHINODERMATA

tentacles protruded, and the young Crinoid begins to feed. The

az.f

FIG. 408. — Fixed larva of Anti'ilmi rnnnci'ii in which the vestibule is open Vint in which
no trace of the arms has yet appeared. (After Carpenter.)

Letters as in previous li^uirs. .•,>•».<, si-iisc-ui xaii mi tcntai/lc.

outer wall of the vestibule splits into five valves (r.v, Fig. 408), each

554

INVEETEBKATA

CHAP.

of which is supported by an oral plate, and the tentacles are protruded
between the valves. The epithelium lining the vestibule becomes
thin, except just over the hydrocoele ring where it becomes thick and
ciliated, and beneath this ring of thickened epithelium a ring of nerve
fibres makes its appearance. The high ciliated epithelium and the
nerve fibres are prolonged over the inner sides of the tentacles.
Sense-organs are scattered over the surface of these tentacles. Each
sense-organ consists of a conical prominence of elongated ectoderm

Fig. 409. — Calyx of larva of about the same age as that represented hi Fig. 408, decalcified
and cleared in order to show the internal structures. (After Ludwig. )

ax, axial or.nan roiitaininj; tin1 t^'nila! stulon ; ub.c, aboral coelom : liii.i; hydrocoele rint; ; m./>, primary
muilreporic pure1 ; or.c, oral coelom ; ur.r, oral valve ; st.c, stone-canal.

cells. The tips of the cells forming the apex of the cone become
elongated so as to form a tactile rod.

The wall separating the aboral coelom and the anterior coelom
thins out till it forms a flat membrane of epithelium, which is then
absorbed and the two cavities which it separated become merged
into one.

In this manner we reach the condition found in the adult
Crinoid, where the stone-canal opens at one end into the general
coelom, and the pore-canal takes its origin independently from this.

XVI

ECHINODEEMATA

555

The "axial organ" becomes a tube, and the vertical mesentery of
the aboral coeloui breaks down into strands.

or.ir

0

Fit;. 410. — Fixed larva of Aitl<i<l<'i<
rosacea viewed from the side in
order to show the origin of the
arms. (After Carpenter. )

AN, anal pink- support in;; flic anus:
R1-R:!, the thii-c railials in a ray Otlirr
liM I IMS as I it-fore.

Beyond this stage Seeliger could not rear his larvae, and here
Terrier's observations may be said to commence ; some splendid

556

INVERTEBRATA

CHAP.

figures are given by Carpenter (1866) of the stages described by this
author. The first stage described by him is the fixed larva with the
closed vestibule ; following on this he has seen the growth of the
arms of the young Crinoid. These arms arise as vertical upgrowths
of the calyx alternating with the oral valves. They are supported

FK;. 411. — View of the calyx of a fixed larva of Antedon rosacea from the upper side, in
order to show the adhesion of the lobe of the hydrocoele to the arm and the first
dichotomy of the arm. (After Perrier. )

a, aims ; n~.t, azygous tentacle formed from thfi tip of the primary lobe of the hydronoele ; n, month ;
r.c, radial canal formed from the liase of the primary lobe of the hydrocoele.

each at its base by a new plate, the primary radial (R1, Fig. 410), and
as they grow in length secondary and tertiary radials are added
(R2, R3, Fig. 410). To these incipient arms the median tentacle in
each radius applies itself and becomes the radial canal of the arm
(r.c, Fig. 411). When the arm forks the tip of the radial canal
remains as an azygous tentacle at the fork, but two branches are

XVI

ECHINODEKMATA

557

Bl

CO

given off just below the tip which become the radial canals of the
daughter arms. In the first dichotomy both arms are equal in size,
but in each dichotomy subsequently one branch remains short and
forms a pinnule but the other grows on and forks again, when the
same process is repeated, so that the apparently single arm of the
Crinoid is really a sympodium formed of a succession of the stronger
members of successive dichotomies. As the arms grow they become
more and more directed outwards, till from their original vertical
they pass into a horizontal position.

Whilst these changes are proceeding secondary stone-canals are
formed, at first one in each of the four interradii not occupied by
the primary stone-canal. Each
of them arises as two solid
buds, one bud being formed in
the outer wall of the coelom
and the other on the hydro-
coele ring. Each of these buds
becomes hollowed out to form
a vesicle. The external one
forms a pore and a thiu-
walled sac communicating
therewith, a replica of the
anterior coelom in fact. The
internal bud forms the new
stone-canal which reaches and
fuses with the vesicle. These
new anterior coelorns soon fuse
with the general coelom, as
did the original one, and so the
secondary stone-canals and the
secondary niadreporic pores
both open into the general
coelom and are disconnected
from each other.

In later stages the new pores and stone-canals do not even reach
one another, and eventually are formed irregularly and independently
of one another, and so the adult condition is reached. The first
branches of the stem, or cirri, are formed just when the first secondary
stone-canals make their appearance. The canals of the chambered
organ expand to form ampullae at the bases of these, repeating the
primitive ampullae at the base of the stem ; and a branch from the
axial organ and the central canal grows out and traverses each
ampulla, and forms a new central canal with its axial organ in the
centre of each cirrus.

These ampullae are really the brain-vesicles of the all-important
aboral nervous system which dominates the movements of the adult.
The cells surrounding them, which are mesenchyme cells budded
from their walls, become converted into the ganglion cells of this

FK;. 412. — Map showing the mutual relations
of the ossicles in the base of the calyx of
a fixed larva of Antedon rosacea when the
adult condition has been nearly attained.
(After Seeliger. )

Bl-B5, tlif live basal ossicles ; SB, the sub-basals ;
a.r, central canal containing tin- axial organ ; c.d
(dotted line), the outline of the adult eentm-clorsal
cell— the plates within this become fuse. I tn^rMiei- ;
eh.o, the live canals of the chambered organ; co/,
the uppermost colunmal.

558 INVERTEBRATA CHAP.

system. The nervous strands which proceed outwards from these
centres are at first merely grooves or gutters in the internal walls of
the calyx. They become shut off from the coelom and transformed
into solid cords of cells which develop sheaths of nerve-fibres. The
mesenchyme cells, by which they are surrounded, become calcigenous
tissue, and thus the original plates of the young Crinoid are increased
in thickness, and in this way the nerves come to lie in the centre of
the radial and brachial plates of the adult. Exactly the same
process takes place with regard to the cirri ; each ampulla of the
chambered organ gives off, as we have seen, a branch leading into
the cirrus, and this branch develops a nervous investment.

The muscles connecting the stem-joints one with another, and
the various ossicles of each cirrus are also formed from mesenchyme
cells ; and the same thing is true of the muscles connecting the arm-
joints with one another. No enibryological distinction can be
perceived between the cells forming the dorsal elastic ligaments of
the arm-joints, which straighten the arms, and the ventral flexor
muscles which bend them, and we are confronted with the remark-
able fact that nervous, muscular, connective, and skeletal tissues
arise from cells of an identical origin.

Meanwhile the portion of the axial organ which is situated in
the calyx has been growing. It becomes plexiform, its original
single tube-like cavity being split into several cavities. Where its
originally lower end reaches the wall of the stomach it gives off five
branches, at first solid but soon becoming hollowed out, one of which
grows into each arm and there forms the genital rachis.

According to Perrier, the septum dividing the oral and aboral
sections of the coelom contained in the arm is a secondary formation,
and has nothing to do with the original septum dividing oral and
aboral coeloms from one another. This may be doubted, and a
re-examination of this point would be desirable. The finished
genital organ is nothing but the apex of the branch of the rachis
which penetrates the pinnule. As in the case of other Echinoderms,
the duct is produced by an outgrowth of the cells of the genital
organ itself, which burrow their way to the outside.

By the secondary thickening of the radial plates, the primary
ampullae of the chambered organ become completely overarched and
shut off from the aboral coelom. The under-basals unite with the
uppermost stem ossicle to form the centro-dorsal ossicle, on which
numerous new cirri make their appearance. This centro-dorsal ossicle
grows till it reaches the primary radials and shuts off the basals
from the exterior. These unite to form a single piece, the rosette
plate, which forms the roof of the chambered organ.

The young Crinoid in this stage, in which arms, pinnules, and cirri
are developed, is termed a Pentacrinoid larva, from its resemblance
to the genus Pentacrinus.

Soon after this the young Crinoid wrenches itself loose from the
stalk, which parts just below the centro-dorsal, and so enters on its

XVI

ECHINODERMATA

559

adult life, when it can swim freely from place to place, and can also
attach itself by its cirri.

When we review the life-history which has just been described,

A

FIG. 413.— The stalked larva and
adult form of Antedon muUi-
spina. (After P. H. Carpenter.)

A, larva. 15. adult. 1i, basal plate ; cir,
cirrus ; //I'M, jiinunli' ; ,-i, tirst radial plate ;
r2, second radial plati- ; r:!, third radial
plate.

cir

we may note, first of all, that some of the stages through which the
young Crinoid passes in its growth, till it loses its stalk, correspond
to the permanent condition in other genera of Crinoidea, both living

560 INVERTEBRATA CHAP.

and extinct. Thus the stalk is retained throughout life in the living
genera Pentacrinus, Rliizocrinus, Batliycrinus, and Hyocrinus, and
in the vast majority of fossil forms. The basals remain exposed in
Thaumatocrinus, Ehizocrinus, Batliycrinus, Hyocrinus, and in an
enormous number of fossil forms. Lastly, in many fossil forms the
under-basals are distinct and exposed, and the nerves running from
the aboral nervous system, instead of being enclosed in the ossicles,
run in open grooves in them.

ANCESTRAL SIGNIFICANCE OF LARVAE OF ECHINODERMATA

We may now pass in review the larvae of Echinodermata viewed
as a whole. We may discount the characteristic features in the
development of Antedon, which are obviously due to the yoiky egg
and incapacity of the free-swimming larva to take food, and regard
it as tolerably certain that, i£ we were lucky enough to find a (Jrinoid
with a small yolkless egg, that this would develop into a larva
fundamentally similar to the larvae of Asteroidea, Echinoidea,
Ophiuroidea, and Holothuroidea. These larvae agree in possessing
as a locomotor organ a folded longitudinal ciliated band with prae-oral
and anal loops ; a V-shaped adoral ciliated band which apparently
removes surplus food from the region of the mouth ; an alimentary
canal consisting of shovel -shaped buccal cavity (stomodaeum),
oesophagus, globular stomach, and intestine ; and a coelom, which
originates as a pouch from the anterior end of the gut, which divides
into right and left halves, and which communicates with the exterior
by a ciliated canal opening on the dorsal surface to the left side of
the middle line.

Now, when we find a group of larvae exhibiting so many characters
in common, we conclude that they represent a common ancestor
from which the groups to which they belong are descended. To this
hypothetical ancestor we may give the name Dipleurula. Since the
larvae in question, so far as their external features go, are perfectly
bilaterally symmetrical, we may regard those of them whose internal
organs exhibit the nearest approach to bilateral symmetry as, in this
respect, retaining the characters of the ancestor. It follows that the
larvae of Ophiuroidea are in this respect most primitive, for it is in
every way likely that the internal asymmetry displayed so markedly
by the Auricularia larva, and in much lesser degree by the Bipinnaria
and the Echinopluteus, is an anticipation of the adult arrangement,
where the organs of the left side overpower those of the right.

We may credit then the ancestral Dipleurula with a coelom
which, on each side, was perfectly or imperfectly divided into three
divisions : an anterior, a middle, and a posterior. The middle
division was prolonged into lobed processes, covered externally with
ciliated epithelium, which projected at each side of the mouth and
produced currents which transported small pelagic organisms, on
which the animal fed, to the mouth. In a word, the two hydrocoeles

xvi ECHINODEKMATA 561

of the ancestor were in every way similar to the lophophoral
arms of Brachiopoda, to the halves of the lophophore of Polyzoa and
of Phoronis, and performed a similar function ; and it must be
remembered that all these lophophores consist of hollow protrusions
of a special division of the coeloni, clothed externally with ciliated
epithelium. The peculiarity of the Echinoderm ancestor was the
anterior coelom with its dorsal ciliated pore ; this, when both
hydrocoeles were equally developed, was also probably double.

No adult animal exactly like this supposititious ancestor at
present swims in the seas, but there are many features of resemblance
between the Dipleurula, whose many features have thus been re-
constructed, and a simple Ctenophore, if we regard the gastro-vascular
canal system as representing a coelom which is still in open com-
munication with the digestive gut, represented in Ctenophores by the
infundibulum or funnel. In Ctenophores the gastro-vascular canal
system consists of an anterior section which is divided into a series of
lobes underlying the ctenophoral canals, and which gives rise to the
canal which leads to the base of the tentacle, and of a posterior section,
the paragastric canal, which runs backwards to the posterior end of
the animal ; there is also an anterior unpaired canal given off from the
upper end of the funnel which terminates in two pores at the anterior
end of the animal. The primitive mouth is not yet divided into mouth
and arms, so that the Ctenophore represents a more primitive con-
dition than our hypothetical Dipleurula. Locomotion is effected by
radiating bands of ciliated epithelium ; and where they converge at
the apical pole there is situated a median neuro-sensory patch of
ectoderm, which is in every way comparable to the organ which
appears in the Echinopluteus larva when it is three weeks old, and
to the sense-organ at the apex of the Crinoid larva.

Now the arrangement of the ciliated ectoderm is very different
in a Ctenophore from what it must have been in a Dipleurula ; still,
if we had before us the Dipleurula and the Ctenophore-like ancestor
of Annelida and Mollusca, when the mouth and arms had become
separated from one another, we should probably have regarded them
as members of the same class of animals. We must remember the
marked tendency of patches of ciliated epithelium to undergo
rearrangement and reunion — as is shown by the production of
transverse ciliated bands in the Auricularia, and in the Crinoid
larva, and in the Echinopluteus of Echinus esculentus, and these
transverse bands do not exactly correspond to one another in any
of these three cases.

It is a fascinating and in every way a likely supposition, that
there existed a class of simple marine animals, distributed all over
the world and diversified into orders, genera, and species, and that
the Ctenophore-like ancestor of Annelida and Mollusca was one
member, and the Dipleurula another member of this class.

If, however, we may draw conclusions from the representations of
these ancestors given us in larval forms, i.e. in the larvae of Echiuo-

VOL. I 2 o

562 INVERTEBKATA CHAP.

derinata on the one hand and in the Trochophore larvae on the other,
there seems to have been a very great difference in the early develop-
ment of these forms. The larvae of modern Ctenophora, and Annelida,
and Mollusca agree in exhibiting in their development the very
early segregation of organ-forming substances in distinct blastomeres,
so that by the time the 4-cell stage is reached a single blastomere
will only produce a quarter embryo. In a word, they exhibit
determinate development. In the eggs of Echinodermata, on the
contrary, the separation of organ-forming substances from one
another takes place at a much later period ; indeed for a considerable
period, in fact until these eggs have attained the blastula stage,
any sufficiently large fragment of the developing egg will regenerate
the whole. That is to say, the development is indeterminate. It
is quite possible that this difference in the character of the early
development distinguished the two ancestors from one another
before anything like modern Ctenophora, Annelida, Mollusca, or
Echinodermata had developed.

We are now faced with the problem as to what interpretation
we are to place on the extraordinary metamorphosis of Echino-
dermata. In searching for this interpretation we must recollect that
a sudden metamorphosis, like that of Echinoidea, in which all the
adult organs are formed under a veil of larval skin and suddenly
break forth into activity, is no safe guide to us. In reconstructing
ancestral history it is an indispensable condition that there should
be continuous and gradual change of function and structure. No
animal ever went to bed, so to speak, with one set of habits and
woke up in the morning with another.

Between, however, the larval free-swimming life and the adult
slow-moving one, there intervenes, in the case of Asteroidea and
Crinoidea, a stage when the animal is fixed by the apex of the
prae-oral lobe which has become converted into a stalk. This fixed
stage suggests a reason for the radial development of organs which is
so marked a feature in the adult Echinoderm. Fixed animals often
develop their external food-catching organs in a radial manner, so
as to sweep the whole neighbourhood for food. But the radial
arrangement of tentacles, as we learn from Coelenterata and Annelida
and Polyzoa, is quite consistent with the retention of bilateral
symmetry. It can only be described as an idiosyncrasy of Echinodernis
that bilateral symmetry is unstable, and that, therefore, radial
symmetry was arrived at by the overgrowth of the organs of the
left side and the partial suppression of those of the right side. To
this day the first sign of uuhealthiness in an Echinoderm larva is
an unequal development of the larval arms.

We may assume, then, that the ancestral Dipleurula took first to
holding on with its prae-oral lobe for short periods, a habit which
became permanent ; and that then the tendency to inequality
between the two hydrocoeles, which we may suppose to have been
latent in the stock, became a positive advantage as a short cut to

XVI

ECHINODERMATA

563

radial symmetry, and was encouraged. But when this stage had
been reached, the study of ontogeny seems to indicate that the
Echinoderm stock became split into two stems. For in Crinoid
development the stomodaeiim, into which the tentacles project, becomes
rotated backwards, so that it eventually occupies the posterior pole

r.pc

mp

FIG. 414. — Diagrammatic reconstruc-
tion of the common ancestor of
the phylum Echinodermata, and
diagrams show the modifications
which the descendants of this
ancestor underwent in becoming
the ancestors of the Eleutherozoon
and Pelmatozoon stocks.

A, Diplmi'uhi aiipi'.stor. B, niici-stm -cif
the Eleuthmi/.uii. C, unrrslur nf Un- Pel-

niuto/oa. a, nuns ; n.c, antiM im- i lorn;

I. hi/, left liyilnirnrlc; /./>.«, left. postninr
coelom ; /»./>, iim'liriioi'ir purr; c./i.i/, ri^ht
; r.p.c, ri.^lit. posterior coelom.

of the body and is directed upwards ; but in Asteroid development the
moutli is moved to the left, and the disc is then flexed on the stalls in
such a wai/ that the mouth looks downwanh.

As a consequence of this flexure, when the hydrocoele ring
becomes completed by the meeting of its two ends, it encircles
the base of the stalk in Asteroidea, but not in Crinoidea, where it is
at the opposite end of the body from that occupied by the stalk.

a

564 INVERTEBRATA CHAP.

It follows that the plates termed "radials" and "basals" in young
.Eleutherozoa and Pelmatozofi do not correspond to each other, but
in each case must be looked on as a rearrangement of scattered plates
when the whole body of the animal had been dominated by pentainerous
symmetry.

Now the change of position which the mouth undergoes in the
metamorphosing Crinoid is quite parallel with the change which it
undergoes in the larva of a Tunicate, or of an Entoproct after
fixation ; and the reason in all three cases is the same, viz. the attempt
to bring the mouth into a more favourable position for catching free-
swimming prey which fill the water above it.

What then can have been the motive for the different shift of the
mouth in an Asteroid ? We can only surmise that it was an adapta-
tion designed to bring the tentacles which surround the mouth into a
more favourable position for grubbing in the mud and detritus on the
substratum surrounding the animal. This supposition accords with
the fundamental distinction which obtains at the present day between
the habits of Eleutherozoa (Asteroidea, Ophiuroidea, Echinoidea,
Holothuroidea), which in the majority of cases are scavengers,
devouring dead animals and organic detritus lying on the bottom,
and those of Pelmatozoa, which to this day feed on Plankton
captured by currents produced by the cilia covering their tentacles.

The difficulty of imagining how a fixed animal could pick up a
living by grubbing in the limited area of mud immediately surround-
ing it, is easily got over if we assume that this mud was not
motionless, but drifting, if, in other words, the ancestral Asteroid had
fixed itself in tide-ways, such as the gaps in coral reefs. Perhaps,
indeed, the original purpose of fixation was to enable the animal to
resist the pull of these tidal currents and avoid being swept helplessly
along. When the old Asteroids extended their range into calmer
water, then the breaking of the stalk would set them free to wander
about and pick up a living under the new conditions.

The post-larval history of both Ophiuroids and Echinoids indicates
that they are derived from the Asteroid stem. In both cases, after
metamorphosis they creep about on their tube feet like an Asteroid,
and in the case of the young Echinoid the terminations of the radial
canals are free movable tentacles, and the dorsal surface, which later be-
comes the insignificant periproct, i^ larger than the ambulatory surface.

We can even form a guess as to what led to the evolution of
these two orders out of a primitive Asteroid. The Ophiuroidea are
merely Asteroidea in which the neuro-muscular system has attained
a higher development. In this respect they are the " highest "
Echinodernmta ; their movements are the most active, and their
sensitiveness the most acute. The Echinoidea, on the contrary, seem
to be a race of "climbing" Asteroidea. The typical regular urchin
loves the vertical faces of stones and the crevices between stones.
These give opportunities to employ the tube feet which spring from
the upper surface of the body.

xvi ECHINODEKMATA 565

The origin of the Holothuroidea is most plausibly explained as a
further development of primitive Echinoidea in the direction of
haunting crevices. Just as the snake has lost its limbs in order to
become adapted to wriggling through crevices, so the Holothuroid
has lost its spines and reduced its plates to vestiges in order to
render its body sufficiently flexible to worm its way through narrow
openings. Synapta forms appropriately the end term in this series
of modifications, for, in this form and its allies, wriggling through
crevices has become changed into burrowing into sand and mud.

If the above interpretation of the developmental history of
Echinodermata be accepted, and it may be fairly claimed to be in
consonance with all the facts so far known, we may draw some
interesting conclusions as to the modifications which the record of
ancestral history, as embodied in ontogeny, has undergone. We see
that a stage of development, viz. the fixed stage, may be completely
omitted, as is the case in Ophiuroidea, Echinoidea, and Holothuroidea,
and in this case the organ of fixation, the prae-oral lobe, is only
vestigially developed ; whilst, on the other hand, certain organs
belonging to the preceding stage, viz. the ciliated band and its
processes, are retained long after the period when, to judge from the
stage of development of other organs, they should have disappeared.

A precisely similar phenomenon is seen in the retention of the
external gills of the salamander after all four limbs have become
adapted for life on land. Further, an organ which should shift from
one position to another by the unequal growth of surrounding parts,
may disappear in one place and be reformed in another, as the mouth
in Asteroidea and Echinoidea. It by no means follows that larvae
which are primitive in one respect are primitive in all. Thus the
Brachiolaria retains a stalk but forms a new mouth, whilst the
Ophiopluteus has no trace of a stalk but retains the old mouth.
Finally, the condition in which development culminates, viz. the
adult condition, tends to be reflected back to earlier and earlier
periods in ontogeny in the case of some organs, and this is what is
termed precocious development.

From all these considerations it follows that different larvae
which reflect in blurred form the same ancestral history, have
become specifically modified ; and this applies not only to larvae
belonging to different classes, such as the Ophiopluteus and Echino-
pluteus, but to the larvae belonging to minor divisions within the
class. Thus the larvae of Spatangoidea seem all to have the aboral
process, whilst those of Ecldnm and its allies are totally devoid of it
but possess ciliated epaulettes. •

Lastly, what preserves a continuous record in ancestral history is
the continuity of functional activity. If this be interrupted all sorts
of aberrancies may occur. Thus the functionless larval gut of Solaster
and Antedon is formed by a secondary development from the coelom,
and the larval stomodaeum is either not formed (Solaster~) or never
reaches the gut {Antedon).

566 INVEETEBEATA CHAP.

LITERATURE CONSULTED

ASTEROIDEA

Agassiz. The Embryology of the Star-fish. Contr. Nat. Hist. U.S., vol. 5, 1864.

Bury, H. The Metamorphosis of Echinoderms. Quart. Journ. Mic. Sc., vol.
38, 1895.

Delap, M. and C. Notes on the Plankton of Valencia Harbour, 1902-1905,
Appendix No. 7, Report on the Sea and Inland Fisheries of Ireland, Part II. (1905).

Field. G. N. The. Larva of Aster ias vulgaris. Quart. Journ. Mic. Sc., vol. 34, 1894.

Gemmill, J. F. The Development of the Star-fish, Solaster endcca (Forbes). Trans.
Zool. Soc. (Loud.), vol. 20, 1912.

Goto. The Metamorphosis of Asterias palUda, with special reference to the Fate of
the Body-cavities. Contr. Zool. Lab. Mus. Com p. Zool. Harvard, No. 98, 1897.

Ludwig, H. Entwicklungsgeschichte der Asterina gibbosa. Zeit. f. wiss. Zool., vol.
37. 1882.

MacBride, E. W. The Development of Asterina gibbosa. Quart. Journ. Mic. Sc.,
vol. 38, 1896.

Masterman. The early Development of Cribrella oculata, with Remarks on
Echinoderm development. Trans. Roy. Soc. (Eclin.), vol. 40, 1902.

Mortensen, Th. Die Echinodermenlarven der Plankton Expedition -nebst einer
system atisch en Revision der bisher bekannten Echinodermenlarven. Ergeb. Plankton
Exped., vol. 2, J., 1898.

OPHIUBOIDEA

Fewkes, J. W. On the Development of the Calcareous Plates of Amphiura squama to. .
Bull. Mus. Com p. Zool. Harvard, vol. 13, 1887.

Grave, C. Ophiura brcvispina. Mem. Biol. Lab. Johns Hopkins, vol. 45, 1900.

Ludwig. Zur Entwicklungsgeschichte des Ophuirenskelettes. Zeit. f. wiss. Zool.,
vol. 36, 1881.

MacBride. The Development of the Genital Organs, Ovoid Gland, Axial and Aboral
Sinuses in Amphiura squamata. Quart. Journ. Mic. Sc., vol. 34, 1892.

MacBride. The Development of Ophiothrix fragil is, ibid., vol. 51, 1897.

Metschnikoff. Studien liber die Entwicklung der Echinodermen und Nemertinen.
Mi'in. Acad. St-Petersbourg, vol. 14, 1869.

Muller. Bericht iiber einige neue Thierformen der Nordsee. Miiller's Arehiv Anat.
u. Pliys., 1845.

Muller. Uber die Larven und die Metamorphose der Ophiuren und Seeigel. Phys.
Abh. Acad. "\Viss. Berlin, 1846.

Russo. Embriologia dell' Amphiura squamata (Sars). Atti Acad. Napoli, series 2,
vol. 5, 1891.

ECHINOIDEA

Boveri. Die Polaritat von Ovocyte, Ei und Larve des Strongylocentrotus lividus.
Zool. Jahrb. (Anat. Out,), vol. 14, 1901.

Bury. The Metamorphoses of Echinoderms. Quart. Journ. Mic. Sc., vol. 38, 1895.

Grave. Some Points in the Structure and Development of Mcllita tcstudinata.
Johns Hopkins Univ. Circ. No. 157, 1902.

MacBride. The Development of Echinus esculentus, together witli some Points in
the Development of J?. miliaris and E. acuius. Phil. Trans. R. Soc. (London), series B,
vol. 195, 1903.

MacBride. The Development of Echinocardium cordaium. Quart. Journ. Mic. Sc..
vol. 59, 1914.

MacBride. Two Abnormal Plutei of Echinus and the Light which they throw on
the Factors in the normal Development of Echinus. Quart. Journ. Mir. Sc., vol. 57, 1911.

Theel, H. On the Development of Echinocyamus pusiUus. Nova Acta P. Soc.
Upsala, 1892.

von tibich. Die Anlage und Ausbildung des Skeletsystems einiger Echiniden und
die Symmetrieverhaltnisse von Larva und Imago. Zeit. f. wiss. Zool., vol. 104, 1913.

von tibich. Die Entwickelung von Strongylocentrotus lividus, Echinus micro-
tuberculatus, Arbacia pustulosa, ibid., vol. 106, 1913.

xvi ECHINODERMATA 567

HOLOTHUROIDEA

Bury. Studies in the Embryology of Echinoderms. Quart. Journ. Mic. Sc. , vol.
29, 1889.

Bury. The Metamorphoses of Echinoderms, ibid., vol. 38, 1895.

Clarke, H. L. tiynapta vivipara, a Contribution to the Morphology of Eohinodemis.
Mem. Bost. Soc. Nat, Hist., vol. 5, 1898.

Ludwig, H. Zur Entwieklungsgeschichte der Holothurien. Sitzber. Akad. Wiss.
Berlin, Jain-gang 1891.

MacBride. On a Collection of young Echinoderms. Nat. Ant. Exped. Nat. Hist.,
vol. «, 1912.

Metschnikoff. Studien iiber die Entwicklung der Echinodennen und Nemertinen.
Mem. Acad. St-lVtrrsbonrg, Series 7, vol. 14, 1869.

Mortensen, T. Zur Anatomic und Entwicklung von Cucumaria glacialis. Zeit,
f. wiss. Zool., vol. 57, 1904.

Muller, J. fiber die Larven und die Metamorphosen der Holothurien und Asterien.
Abh. Akad. Wiss. (Berlin), 1850.

Selenka. Studien iiber die Entwicklungsgeschiehte der Thiere. Heft II. Die
Keimblatter der Echinodermen (Wiesbaden), 1883.

Selenka. Zur Entwicklung der Holothurien. Zeit. f. wiss. Zool., vol. 27, 1876.

Semon. Die Entwicklung der Synapta digitata und die Starnmesgeschichte der
Echinod(>rmen. Jen. Zeit., vol. 22, 1888.

Semon. Die Homologien innerhalt des Echinodermenstammes. Jen. Zeit., vol.
22, 1888.

CRINOIDEA

Bury. The Early Stages of the Development of Antcdon rosacca. Phil. Trans. R.
Soc. (Loud.), Series B, vol. 179, 1888.

Carpenter, W. Researches on the Structure, Physiology, and Development of
Antedoii (Comatula] rosacea. Phil. Trans. R. Soc. (Lond. ), vol. 156, 1866.

Perrier. Memoire sur 1'organisation et le developpement de la Comatule de la Medi-
teiTiiuee. Nouv. Arch. Mus. His. Nat. Paris, vol. 10, 1889.

Seeliger, O. Studien zur Entwicklungsgeschiehte der Crinoiden (Antcdon rosttcea).
Zool. Jahrb. Anat., vol. 6, 1892.

EXPERIMENTAL

Driesch, H. Entwicklungsmechanische Studien, I. II. Zeit. f. wiss. Zool., vol. 53,
1892 ; III. IV., itiiil., vol. 55, 1895.

Driesch, H. Zur Analysis der Potenzen embryonaler Organzellen. Arch. Ent. -Mech.,
vol. 2, 1895.

Driesch, H. Die isolierten Blastomeren des Echiniden-Keimes, ibid. , vol. 10, 1900.

Godlewski. fiber die Bastardierung der Echiniden- und Crinoidenfamilien. Arch.
Ent. -Mech., vol. 20, 1906.

Herbst, C. Experimentelle Untersuchungen iiber den Einlluss der veranderten
ohemischf Zusammensetzung des umgebenden Medium auf die Entwicklung der Thiere,
Pt. I. Zeit, f. wiss. Zool., vol. 55, 1893 ; Pt. II., Mitt. Zool. Station zur Neapel, vol.
2, 1895 ; Pt. .III., Arch. Ent.-Mi'ch., vol. 2, 1896.

Herbst. Uber das Auseiuandergehen von Furchung und Geweheszellen in kalkfreien
Medium. Arch. Ent, -Mech., vol. 9, 1900.

Kupelwieser. Entwicklungserregung bei Seeigeleiern durch Molluskensperma.
Arch. Ent, -Mech., vol. 27, 1909^

Loeb. Die chemische Entwicklung des tierischen Eies. Jena, 1910.

MacBride. The Early Larva of Echinoc.ardium conlatum and the result of crossing
this Species with Echinus esculcnt.us. Quart. Journ. Mic. Sc., vol. 58, 1912.

Seeliger. Gibt es geschleclitlich erzeugte Organismen ohne miitterliche Eigen-
schaften? Arch. Ent.-Mech., vol. 1. 1894.

Shearer, C., Fuchs, H. M. , and De Morgan. On Paternal Characters in Echiimid
hybrids of Echinus. Quart. Journ. Mic. Sc., vol. 55, 1912.

CHAPTER XVII
PKOTOCHOKDATA

Classification adojited—

Hemichorda (Enteropneusta)
Cephalochorda

Urochorda (Tunicata)

Larvacea

[Ascidiae simplices
Ascidiacea Ascidiae compositae

'Ascidiae Luciae
IThaliacea

ALTHOUGH the second and third volumes of this work are destined
to treat of the embryology of the great group of Vertebrata or
Chordata to which we ourselves belong, yet it is necessary to deal at
the close of this first volume with the embryology of the lowest
members of this group, for two reasons. First, because we must show
how the Vertebrata are related to the Invertebrate groups whose
embryology has been discussed in this volume ; and, secondly, because
one of the three groups which make up the division of Vertebrata
known as Protochordata are still frequently regarded as Invertebrata.
The Vertebrate affinities of the Enteropneusta are denied by
many zoologists, and although all now admit that the Urochorda
are degenerate Vertebrata, yet these animals are so degenerate that
their adult structure shows more similarity to that of a Podaxonian
or Polyzoan than to that of any ordinary Vertebrate. The name
Protochordata is, of course, nothing more than a convenient collective
term for the poor relations of the vertebrate phylum which fall far
below the rest of their brethren in structure and activity. It is by
no means implied that its three subdivisions — Hemichorda, Cephalo-
chorda, and Urochorda— are specially closely allied to one another.
What indeed their relationship to one another actually is, will come
out when their life-histories are studied.

We prefer the term Vertebrata to Chordata for the following

568

CHAP, xvn PEOTOCHOEDATA 569

reasons: — The word "Vertebrata" is so deeply established in the
literature that it is impossible to eradicate it. If all Vertel >rata must
have true vertebrae, then not only must the groups classed as Proto-
chordata be ejected from the phylum, but also Cyclostomata, Elasnio-
branchii, Dipnoi, Chondrosteid Ganoids amongst fish, and the lower
Stegoceplrila amongst fossil Amphibia. If Amphioxus be "a-centrous"
so also is the sturgeon. We must not draw a line which will bifurcate
natural groups, hence the name "Vertebrata" must apply to the
whole group of animals characterized by dorsal tubular nervous
system, notochord, and gill-slits.

HEMICHORDA — ENTEROPNEUSTA

The Enteropneusta are represented at the present day by two
totally distinct types of animal, both of which are marine. One, the
Balanoglossida, resemble in outer appearance " worms," like Nemertea
or Annelida, and lead a burrowing life, inhabiting the soft mud at
the bottom of shallow waters all over the tropical and temperate
regions of the world ; whilst the other type, the Cephalodiscida, are
sessile colonial animals, very much resembling Polyzoa in appearance
and habit of life, and confined to the colder temperate, arctic, and
antarctic regions of the sea. They were indeed, until very recently,
confounded with Polyzoa.

About the embryology of the Cephalodiscida practically nothing
is known ; on one occasion when a fresh colony was dredged by a
vessel proceeding on a voyage of Antarctic exploration, it was seen to
emit oval ciliated larvae. The subsequent death of the naturalist
attached to this vessel has prevented this most interesting discovery
from being adequately followed up.

Of the development of the Balanoglossida, however, we know a
great deal more. Long ago it wras discovered by Me tschnik off (18*70)
that a remarkable larva named Tornaria, which had been frequently
captured in the Plankton by the tow-net, and which had been mis-
taken for the larva of an Asteroid, was really the larva of a Balano-
glossid worm. Then Bateson (1884-1885) worked out completely
the life-history of a form, Balanoglossus (Dolichoglossus) Kowalevskii,
which has somewhat yolky eggs and a shortened larval development.
This development bears much the same relationship to the life-cycle
which includes the Tornaria larva as does the development of Asterina
gibbosa to that of Asterias with its biphmaria larva.

Bateson's work, which is the foundation of our accurate knowledge
of Enteropneust development, and which led to the view that the
Enteropneusta have vertebrate affinities, was challenged by Spengel
(1894), who questioned its accuracy and founded a view of the
relationship of the Enteropneusta with Annelida on his own observa-
tions on Tornaria larvae. It is therefore important to notice that
Bateson's conclusions have been confirmed, clarified, and reinforced
by a series of researches executed by American zoologists, of whom

570 INVEETEBKATA CHAP.

the most noticeable are Morgan (1891, 1894), who worked out the
later development of several varieties of Toruaria which occur on the
east coast of North America ; Eitter (1894), who described stages of the
development of a species of Tornaria from the Pacific coast of North
America; and Davis (1908), who described the development of
a Balanoglossid (Dolichoglossus pusillus), with yolky eggs and
shortened development, which appears to be closely allied to the
species on which Bateson worked. Finally, a German, Heider (1909),
has succeeded, for the first time, in obtaining the fertilized eggs of a
Balanoglossid (Balanoglossus clavigerus}, which has in its life-cycle a
Tornaria larva ; and he reared the eggs until the typical Tornaria
larval form had been attained.

BALANOGLOSSUS

A fairly complete account of the development of a Balanoglossid
can therefore be pieced together by adding Heider's work to that of
Morgan. It is probable that the New England Tornaria belongs to
some other species of the genus Balanoglossus. We prefer to take
the researches of these two workers as the basis for our detailed
account rather than to base our account on the development of
Dolichoglossus, as worked out by Bateson and Davis, because we hold
that a roundabout development, including the formation of a pelagic
larva with a long free-swimming existence, is the primitive type of
development, and that a shortened development with a larva having
a very short free-swimming life, and in which the adult features
appear very early, like that of Dolichoglossus, is a secondarily modified
condition of affairs.

Heider obtained the fertilized eggs amongst a consignment of the
adults which were collected at the Zoological Station at Trieste and
sent to him at Innsbriick. During the journey males and females
discharged their genital products and a natural fertilization (see
p. 485) resulted. Subsequently, when on their arrival the adults
were placed in sea-water with sand at the bottom, they formed burrows
in it, and at the mouth of one of the burrows a slimy mass contain-
ing thousands of eggs was seen. These eggs, however, were not
fertilized.

The eggs were small and filled witli coarse giains of yolk which
were uniformly distributed, so that the only way of distinguishing
animal and vegetative poles was the nearness of the egg-nucleus to
the former. In the fertilized eggs the usual two polar bodies were
formed, of which the first divided.

The eggs segmented with perfect regularity into blastomeres of
equal size, and gave rise to perfectly spherical thick-walled blastulae,
with comparatively small blastocoeles whose walls were composed of
a very large number of narrow, cylindrical, ciliated cells. Heider
considered that the development up to this point recalled that of
Echinoidea, but the Balanoglossid blastula differs from the Echinoid

XVII

PROTOCHOEDATA

571

blastula in having thicker walls. Further, it is composed of taller
cells than the latter blastula. In both cases, however, it is obvious
that we have to do with indeterminate cleavage ; nothing even dis-
tantly suggesting the spiral cleavage of Annelida is to be seen.

The blastula stage had been already attained by the vigorous eggs
when the material came into Heider's hands. On the following day
the blastulae became hemispherical, by the flattening of one side,
as do Echinoid blastulae, and the gastrula stage was attained
by the imagination of this flattened surface. The archenteron did
not completely fill up the blastocoele, since, coincidently irith its

coe1

FIG. 415. — Early stages in the development of Bdlanmjlossux cluri'/i-riift. (After Heiiler. )

A, Blastula (about one day old). 13, incipient .yastrulation (uric and a halt' days old). C, gastrula
(two days old). D, formation of tin- anterior oieloin. lilji, blastopore ; cue1, anterior coeloni.

formation, the embryo grew in length. The blastopore was at first
wide, but became reduced to a narrow pore and finally closed altogether;
but the endodermic sac remained connected with the ectoderm at the
spot where the closure took place, and here, at a slightly later stage,
the anus was formed ; so that we may say that in Balanoglossus clavi-
gerus the blastopore becomes the anus, but for a brief period it is closed.
The front end of the somewhat elongated embryo then broadened
out, and the whole organism became flattened so as to have broad
dorsal and ventral surfaces and narrow sides. The front portion of
the archenteron became separated from the rest by a, groove, and so
constituted the anterior coelomic vesicle, the rudiment of the pro-
boscis coelomic cavity of the adult (Fig. 415). The cells forming the

572

INVERTEBRATA

CHAP.

wall of this sac lost their cylindrical form and became flattened, and
sent out pseudo-podia by which the coelomic sac was anchored, so to
speak, to the ectodermal walls of the body.

The anterior coeloni now sent out a prolongation which reached
the anterior pole of the embryo ; at this point an apical plate was

coe1

FIG. 416. — Later stages in the development of Balanoglossus clavigerm. (After Heider.)

A, formation of the apical plate. B, formation of mouth anil of pore-canal. C, mouth anus and
water pore formed, a, anus; ap, apical plate; fuel, anterior cni'lom ; int. intestine; <>, mouth; oes,
endodermal section of oesophagus ; p.c, pore-canal ; rf, stomach ; *ttnn, stoniudurum ; cy/i,

formed by a thickening of the ectoderm, and the cells forming this
thickening developed long stiff cilia, so that in this way a typical
apical plate was formed. From the coelomic sac also a dorsal pro-
jection was developed which grew backwards and fused with the
ectoderm, and here, somewhat later, an opening was effected which
became the proboscis-pore or water-pore of the adult (w.p, Fig.
416, C).

XVII

PEOTOCHOEDATA

573

The front end of the gut, as we may term the remnant of the,
archenteron, now became bent towards the ventral surface, and here
came into contact with the ectoderm ; this ventral prolongation con-
stitutes the rudiment of the larval oesophagus. At the same time
the hinder part of the gut exhibited the constriction separating a
globular stomach from a narrow intestine.

At this stage, reached one and a half days after the blastula stage
had been attained, the embryo burst the egg-membrane and began its
career as a free-swimming larva which was uniformly ciliated all over.
On the next day both mouth and anus broke through ; there was a
very shallow wide stomodaeum similar to but much shallower than
the stomodaeum of the Echinoderm larva, but almost all the

ap

mes

mux

oes

mt

FIG. 417. — Still later stages in tlie development of Balanocjlossus clavigerus.

(After Heider.)

A, formation of mesenchyme. B, retreat of anterior coelom from apical plate, and formation of
apical string, up, apical plate ; nyi.s, apical string ; rue1, anterior coelom ; int, intestine ; »«<•.<, mrsrn-
cliymr cells; «M«C, muscular fibrils — outgrowths of nifsrnchyme cells; uc, eye-spot ; >«.<, oesophagus ;
s/, stomach ; H-.II, \vater-poi e.

oesophagus was of endodermal origin. Oesophagus, stomach, and
intestine were now sharply marked off from one another, and the
whole interior of the alimentary canal was ciliated. The anterior
prolongation of the coelomic sac became solid and so formed the
apical string (ap.s, Fig. 417, B), which connects the apical plate
with the proboscis-coelom and with the oesophagus, and on the next
day its cells developed contractile fibrils, and the string was thus con-
verted into a muscular strand. From this string were also given off
the first mesenchyme cells which wander into the blastocoele. These
consequently originate at a later stage of development in this larva
than in any Echinoderm larva studied. Where the posterior aspect
of the vesicle touched the oesophagus, pseudopodium-like strings
grew out from its cells which were converted into circular muscles
(muse, Fig. 417, A), and we may remind our readers that the circular
muscles of the oesophagus of the Echinopluteus larva are formed in
a precisely similar way.

574

INVEETEBEATA

CHAP.

Heider was able to keep the larvae living for eight days. Though
still ciliated all over, a concentration of ciliated cells was observable
along certain lines corresponding to the position of the ciliated bands
of the full-grown Tornaria larva ; these are a longitudinal folded
band with a marked back wardly directed prae-oral loop, in all respects
similar to the main ciliated band of a young Bipinnaria larva, and a
posterior transverse ciliated band which is the main external feature
which distinguishes the Tornaria larva from the young Bipinnaria

and Auricularia larvae. This band
corresponds roughly in position
to the telotroch of Annelid larvae
and will receive the same name,
viz. telotroch (ttr, Fig. 418). The
apical plate had by this time
developed two eye-spots which
were simple cups of ectoderm cells
surrounded by pigment. The plate
is situated just at the spot where
the prae-oral loop originates from
the main part of the longitudinal
ciliated band. The anterior coelom
now sent out two posterior spurs
which arched round the oesophagus,
and in. the oldest larvae Heider
was able to detect the origin of a
pair of posterior coelornic vesicles
which form the rudiment of the
trunk -coelom. These arose as
evaginations, with slit-like luniina,
of the anterior wall of the intestine,
just behind the groove which
marks it off from the stomach.

Morgan's observations (1891)
on the development of the New
England Tornaria commence
just at the stage where Heider's
observations leave off. His material consisted of a swarm of
Tornaria larvae of all ages which were caught by the tow-net off
Wood's Hole, Massachusetts, in the summer of 1890. The youngest
of these were only ^ mm. long, but in them the anterior coelom was
entirely separated from the gut and the proboscis-pore had been
formed. The two ciliated bands were distinct, but the anterior one
was barely folded. The posterior coelomic sacs had not yet been
formed. The apical plate was completely fused with the sides of the
longitudinal baud at the prae-oral pole of the larva, where these sides
approach most closely to one another ; it thus formed a bridge
delimiting a prae-oral loop from the rest of the band. On the apical
plate were two eye-cups, an anterior and posterior. These were

ttr

FIG. 418. — Surface view of the young
Tornaria larva of Balanoglossus cf " ri-
ff er us, four days old. (After Heider.)

(i, anus; n//, apical plate ; cil.lnnij, longitudinal
kind of cilia ; «, mouth ; oc, eye-spots ; ttr,
telotroch, i.e. posterior transverse band of cilia.

XVII

PROTOCHORDATA

575

hemispherical pockets of clear cells, each cell terminating in a conical
spike. Between the two eye-cups were a mass of pigmented cells.
At the base of the apical plate a mass of nervous fibrils could lie seen
(Fig. 419).

In somewhat older larvae a solid mass of cells could he seen lying
in the blastocoele, above and somewhat to the right of the proboscis-
pore. These cells, whose origin Morgan could not determine, we
conclude, from the development of Dolichoglossus, have been derived
from the posterior wall of the anterior coelom. They are the rudi-
ment of the pericardium, for in a slightly older larvae they became

Fie. 419. — Illustrating the structure of the apical plate and eyes of a full-grown
New England Tornaria larva. (After Morgan.)

A, apical view of full-grown Tornaria, showing the apical plate and eyes, and the relation of the plate
to the longitudinal ciliated band. B, antero-posterior longitudinal section through the apical plate ami
eyes, cil.long, longitudinal ciliated baud ; »<««-, muscle cells belonging to the apical string; OCM,
anterior eye ; w.ji, posterior eye.

hollowed out to form a vesicle (per, Fig. 421). Between this vesicle
and the oesophagus and the posterior wall of the anterior coelom there
existed a V-shaped space, tilled with blastocoelic fluid and opening
into the blastocoele behind. This space is the rudiment of the peculiar
dorsal heart of Balanoglossida, which has been seen to pulsate.

In larvae older than the second stage described, the posterior
or trunk coelomic cavities could be seen developing exactly as
Heider described in the case of Balanoylossus clavigerus. Slightly
later, the middle, or collar coelomic cavities originated as solid
evaginations of the posterior part of the wall of the stomach (Fig.
420). Both pairs of rudiments, after being cut off from the alimentary

576

INVERTEBEATA

CHAP.

coe-

canal, formed, for a time, little solid disc-like bodies applied to the
sides of the stomach and intestine. Only very gradually did they
acquire distinct lumina, and extend dorsally and ventrally so as to
encircle the gut and meet their fellows in the mid-dorsal line. Their
extension in an antero-posterior direction was very restricted until
the very close of larval life.

When we examine the structure of the full-grown Tornaria larva
before metamorphosis sets in, we find that the longitudinal band of
cilia, in addition to becoming differentiated into prae-oral and post-
oral loops, has been thrown into several secondary folds which we

may term arms. If we applied
the nomenclature which Mor-
tensen has invented for Echino-
derm larva (see p. 464), we
should say that the longitudinal
band, in addition to giving off
a backwardly directed prae-
oral loop, gave off also a
forwardly directed anal loop.
Where the anal loop is given
oil' there is, on each side, a
conspicuous postero - lateral
arm of the band. From the
sides of the prae-oral loop a
large prae-oral arm is given
off, and on the main portion
of the baud, just behind this
loop and behind the apical
plate, is also to be
1 tackwardly directed
dorsal arm ; on the left side
is the proboscis-pore.

The ventral ectoderm form-
ing the oral field, included
between prae-oral and anal
loops, is thin and flat. Outside this area it is composed of cubical
cells, and it becomes quite thick on the anterior part of the larva
around the apical plate, and to a lesser extent around the anus
within the area included within the posterior ciliated band. The
epithelium lining the dorsal and ventral walls of the. oesophagus
is ciliated ; the dorsal cilia stop short of the stomach, but the ventral
ciliated band is continued into the general ciliation of the walls of
the stomach.

The sides of the oesophagus are produced into several pairs of
pockets, these are the rudiments of the future gill pouches (g.p,
Fig. 421). It will be particularly noted that in the Tornaria larva
the gill region is far in front of the middle or collar body -cavity
which embraced the hinder end of the stomach, whereas in the adult,

Fi<;. 420. — Illustrating the origin of the middle

and posterior coelomic vesicles in the New

England Tornaria. (After Morgan.)

A, longit uiliiial section through the anterior portion

of the wall of the .stomach, in order to show the origin

of the collar cavity. B, longitudinal section through

the posterior portion of the wall of the stomach, anil

through the wall of the intestine, in order to show

the origin of the trunk-cavity. coea, rudiment of collar-

cavity ; i-m"; rudiment of trunk-cavity ; int, intestinal

wall ; xt, stomac-h wall.

found a
antero-

xvn PBOTOCHOEDATA 577

the gill region is behind the collar-cavity altogether. The stomach
and intestine are separated by a diaphragm perforated by a hole,
round which is a wisp of long cilia which beat so as to produce
rotatory movements..

As metamorphosis draws on the larva decreases in size and
becomes more opaque. These changes are due to a diminution in
size of the blastocoele and to a change in shape of the ectoderm cells,
which become more columnar. The longitudinal band of cilia
becomes indistinct, except along its posterior border ; the circular
band remains active, but it becomes shifted farther back by a growth

ff-P

oes.

proa

a

FIG. 421. — Full-grown New England Toruaria seen from the left side. (After Morgan.)

c, anus; ii.il.ii, anterior dursal arm of the longitudinal ciliated band; 0/1, apical plate; r»/<..s, apical
string ; til.lung, longitudinal ciliated band ; coe1, anterior (proboscis) coelom ; m&, middle (collar)
coelom; COR*, posterior (trunk) coelom; q.p, gill pouches ; iitt, intestine; o, mouth; oes, oesophagus;
j>cr, pericardial sac ; p.l.n, posterior lateral arm of the longitudinal ciliated band ; pr.o.a, prae-oral arm
of the longitudinal ciliated band ; st, stomach ; /./;-, telotroch ; u:p, water-pore.

of the region of the body intervening between it and the longi-
tudinal band.

The larva now drops to the bottom and glides over it by the
help of the cilia of the circular band. The anterior region of the
body grows in length and becomes conical, and gradually takes on
the shape of the proboscis of the adult. The posterior wall of the
anterior coelom or proboscis-cavity becomes curved forwards and
thrown into a number of folds, and this constitutes the excretory
tissue or head kidney <>f the adult (ex, Fig. 422, A and B). The
posterior border of the longitudinal band becomes slightly invaginated
and marks the front edge of the collar region ; the hinder limit of
this region is marked by a new transverse groove, which now appears

VOL. i 2 p

578

INVERTEBRATA

CHAP.

on each side and passes forwards near the mid-dorsal line to join the
groove marking the front border of the collar. In the mid-dorsal line
there is consequently a strip of ectoderm uncrossed by the grooves.

ex

FIG. 422. — Illustrating the metamorphosis of the
Bahamas Tornaria. (After Morgan.)

A, Tornaria just before the metamorphosis. B,
Tornaria during the metamorphosis. C, Young Balano-
glossid worm with three pairs of gill-slits, op, apical
plate ; c! I. long, degenerating longitudinal ciliated band ;
oo?, collar region; col.p, collar-pore; cr, excretory tissue
in posterior wall of proboscis coelom ; f/./>, end»dei mie
gill pouch ; r/.x, gill-slit ; pr.p, proboscis-pore ; t.li, tongue-
bar dividing the gill-slit; t.tr, telotroch; f.M, accessory
fell it inch characteristic of the Bahamas larva.

This is the rudiment of the dorsal neural plate. It becomes depressed
beneath the surface, flaps of the adjacent ectoderm, which we may
term neural folds, meet over it, and in this way a dorsal neural
tube is formed (n.t., Fig. 423).

XVII

PEOTOCHOEDATA

579

About this time, from the anterior end of the oesophagus, a
median dorsal, forwardly-directed pouch grows out ; this is the
rudiment of the notochord (Fig. 424). Transverse sections show
that this pouch is continued backwards as a dorsal section of the
oesophagus, separated by lateral grooves from the rest, and that in
these grooves lie two chitinous rods secreted byoesophageal epithelium.
These are the legs of the collar
skeleton, which is merely a
specially thickened portion of
the cuticle secreted by the bases
of the notochordal cells, and
corresponds to the primary
cuticular sheath of the notochord
of higher Vertebrata. The gill
pouches become applied to the
ectoderm, and here the external
gill openings are formed. Tongue
bars, i.e. vertical folds of the dor-
sal walls of these pouches, dividing
these cavities almost into two,
are formed before the external
openings appear (t.b, Fig. 422, C).

The larva has now almost
assumed the form of the adult,
but a remarkable change in the
dimensions of the gut has yet
to make its appearance. This
has been described as a " pulling
in" of the anterior portion of
the £ut • but it might be more

o ' *•— '

aptly described as a lengthening
of the region in front of the
gills. As a consequence the gills
become pushed back till they
lie behind the collar region, the

diaphragm Separating Stomach A' '^'-section through the nervous system of

i . o a younger specimen — the nerve plate is flanked liy

and intestine disappears, and two ectodermic folds. B, i-r<>ss-s..(-ti<»n through

tlin nervous system of an older siieeimeii — the
ectodermic folds have ni>'t above tlir IMTM- plate
and the nerve plate has lieeome a ner\e tulie. «.//,
nerve plate ; n.t, nerve tubr.

FIK. 423. — Illustrating the development of
the dorsal nervous system in the meta-
morphosing Bahamas Tornaria. (After
Morgan. )

these two regions are conse-
quently no longer distinguishable.

Morgan was able to keep his
oldest Tornaria larvae alive for

three days after they had been caught, and to watch them metamor-
phose as has been described, but he did not see them begin to burrow.
Subsequently he visited the Bahamas and found there, in the Plankton,
two much larger varieties of Tornaria, the metamorphosis of one of
which (the Nassau Tornaria) he was able to study in some detail.
His results are recorded in a second paper (1894).

This larva differs from the New England one, not only in its much

580

INVERTEBRATA

CHAP.

greater size, but in the elaboration of the processes of its longitudinal
ciliated band. The sides of the prae-oral loop and of its outgrowths,
the prae-oral processes, as well as the sides of the main portion of the
longitudinal ciliated band and of its outgrowths, the antero-dorsal
processes, are fringed with small, secondary, finger-like processes.
There is also a second circular band of cilia behind the telotroch, but
much more feebly developed. According to Morgan, in this larva

ap.n

ch

oes

coe

tlr

coe

int

FIG. 424. — Longitudinal sagittal section through the New England Toruaria immediately
after its metamorphosis into the Balanoglossid worm. (After Morgan.)

nil. a, nervous tissue underlying the apical plate ; i-/i, rudiment of notuchord ; cue1, proboscis coelom ;
coe2, collar coelom ; fur*, trunk coelom ; int, intestine ; n.p, dorsal neural plate in the collar region ; («•.<,
ursuphagus ; p.wl.g, posterior collar groove ; nt, stomach; t.tr, telotroch.

the collar-cavities originate by the aggregation of scattered inesen-
cliyme cells. This statement is in the highest degree improbable ;
such an impression might be produced on the mind of an observer if
the critical stages of the development were missed out.

The principal additional points which Morgan made out satis-
factorily in these larvae were, the formation of the collar pores, and
the first traces of the genital organs. The collar pores originate
as two ectodermal invaginations situated on the sides of the body, not
far from the mid-dorsal line at the hinder region of the collar. The

XVII

PKOTOCHOKDATA

581

gon

tips of these imaginations become fused with the collar coelorn on
either side, and here the collar pores are formed. The first and second
pairs of gill pockets also open into these invaginations, which Morgan,
following Batesou, compares to
the atrial cavity of Amphioxus.

The genital organs, which
in Balanpglossida are very small
and numerous and widely
scattered, and of which each
possesses its own duct, originate
as local proliferations of the cells
forming the outer walls of the
trunk coelom (gon, Fig. 425).

The thickened hand of ecto-
derm cells, marking the site of
the posterior ciliated hand, per-
sists for a long time in the
Bahama larva ; and it is possible
to make out that the trunk of
the young Balanoglossid worm
is made up, in about equal
proportions, of the regions in
front of and behind this band,
in both of which very great
growth in length takes place.

Morgan was able to see the
young metamorphosed forms
burrowing into the mud at the
bottom of his culture vessels.

The Tornaria found by Bitter
(1894) on the Pacific coast of
North America, agrees with the
Bahama form in having secondary
processes (tentacles) developed
along the course of the prae-oral
processes, and also on the main
part of the longitudinal band,
but these processes are fewer in
number and blunter than in the
Bahama larva. There is also an
additional pair of processes on
the horizontal part of the longi-
tudinal band, situated near the
mid-ventral line which, following Mortensens' notation, we may name
post-oral. As in the Bahama larva there is a second transverse
band of cilia situated behind the first main one.

In this Tornaria, in the mid- ventral wall of the oesophagus there
is a thick ridge carrying especially long cilia. This ridge is compared

Fi<;. 425. — Portions of transverse sections
through the trunk region of three young
Balanoglossid worms of different ages, in
order to illustrate the development of the
genital organ in the Bahamas species.
(After Morgan.)

cm-", trunk-cavity ; ;/<>», developing genital (n.^ni.

582 INVEETEBEATA CHAP.

by Eitter to the endostyle of Ampliioxus ; it is apparently continuous
with a lesser ridge of the same kind in the wall of the stomach.
The nerve plate is converted into a nerve tube in exactly the same
manner as in the New England Toruaria.

1 DOLICHOGLOSSUS

We must now devote some consideration to the shortened
development of Dolichoglossus as worked out by Batesoii and Davis.
Bateson (1884-1885) found that the eggs of the species he worked
at (I). JcowalevsJcii), were shed into the soft mud which the parent worm
inhabited, and there passed through the whole of their development.

The eggs were comparatively large (about '4 mm. in diameter),
filled with a yellowish yolk and provided with a firm egg-shell.
Attempts at artificial fertilization led only to abnormal segmentation
and death of the embryo, and so all stages of development had to be
procured from the mud, and Batesoii's method of finding them was
not a little ingenious. He procured a quantity of mud in which the
adults lived, and to this was added a number of adult worms cut into
small fragments ; the whole mixture was stirred up with sea- water,
avoiding rotatory currents. Then, after waiting a minute or two to
allow the agitation to cease, the upper layers of the fluid were
siphoned off until the layer containing the fragments of the adult
worm was reached. This layer was then siphoned off and carefully
preserved. In it were found the fertilized eggs and the embryos and
larvae in all stages of their development, since all these were about
the same specific gravity as the fragments of the parent worm.

The embryos in their early stages of development agree precisely
with the embryos of Balanoglossus clavigerus as described by Heider.
The proboscis coelom is formed as in the Tornaria larva, but the
collar and trunk coelomic cavities arise about the same time as
hollow evaginations of the gut. When the larva escapes from the
egg-membrane, the same stage of development has been attained as
is reached by the Tornaria larva just before its metamorphosis. The
larva possesses an apical tuft of cilia, and a ciliated band encircling
the posterior region of the body, evidently homologous with the
telotroch in the Toruaria larva. The whole ectoderm is beset
with shurt cilia, but there is 110 trace of the characteristic folded,
longitudinal ciliated baud of the Tornaria larva. Two transverse
grouves, including between them a narrow transverse ridge, have
appeared. This ridge is the rudiment of the collar region. Some
distance behind this the first gill-pore appears on either side ; but
the collar region grows back till it covers not only this gill-slit, but
also the second which is subsequently formed.

The changes necessary to reach the adult condition are few ; the
apical tuft and posterior ciliated band disappear, the prae-oral portion
of the larva grows in length and becomes conical, the gill-slits increase
in number, and the trunk region grows in length.

XVII

PROTOCHORDATA

583

The pericar dial vesicle originates as a solid outgrowth of the posterior
horn of the proboscis-cavity ; and the dorsal nerve cord is delaminated as
a solid strip of ectoderm, into which canals extend, subsequently from
tli.r. anterior and posterior ends of the collar where it remains in
connection ivith the ectoderm.

Davis' account of the embryology of D. pusillus (1908) agrees
in many points with Bateson's account of the development of D.
koiualevskii, which we have just summarized. The embryo hatches
out and begins free life when the collar region is delimited and one
pair of gill-pores has appeared.

Owing to the fact that the mud was of a more cohesive kind
than that in which D. koivalevskii lives, it was possible, at low tide,
to take spadefuls of mud containing the
burrows intact, and when these burrows
were broken open the fertilized eggs were
seen clinging to one side of them. A
mixture of corrosive sublimate and acetic
acid, osmic acid, and Lo Bianco's chrom-
osmic mixture, were used for preserving
the embryos. The embryos and larvae,
which were removed from the burrows,
lived and completed their development in
vessels of clean water in the laboratory.

When the larvae are first hatched
they swim in spirals and rise to the
surface, but soon tire and drop to the
bottom (Fig. 426). These swimming
efforts at first occur at regular intervals,
but the intervals become gradually longer
and longer, and finally the larvae only FK;. 426.— The larva of
glide over the bottom. Soon muscular giossus pwaim in the act of
movements are observable in the proboscis,
and with the loss of cilia the burrowing
life of the adult is begun. These
spasmodic upward movements, however,
give opportunities to the tidal current to waft the larvae far from
their birthplace.

The principal points of interest in the development of D. pusillus,
as brought out by Davis, are as follows: (1) The cleavage is not
quite regular, for, as in the egg of Amphioxus, the upper four blasto-
meres of the 8 -cell stage are smaller than the lower four, and
there is a cleavage pore ; that is to say, that the incipient blastocoele,
formed by the separation of the blastomeres, opens above and below.
(This also occurs in the egg of Amphioxus.') (2) Both middle and
posterior pairs of coelomic cavities arise as outgrowths of the anterior
body-cavity, so that, as in Echinoderms, there is one anterior
e vagina tion. of the archenteron which gives rise to all the body-
cavities (Fig. 427).

escaping- from the egg-membrane.
(After Davis. )

"/>. apical jilafr ; <W, collar region ;
e.m, c'uu-iiii'inljiaiii' ; t.ti-, tclotrocli.

584

INVERTEBEATA

CHAP.

AFFINITIES OF THE ENTEROPNEUSTA.

The question of the vertebrate affinities of the Euteropneusta
stands or falls with the homology of the nerve cord, notochord, and
gill-slits with the similarly-named structures in the higher vertebrates.
Our own view, that the two sets of structures are really homo-
logous, and that Eiiteropneusta are a degenerate offshoot from the
base of the vertebrate stem, will be supported by evidence given
when the development of the Cephalochorda is discussed, "since
these are the lowest forms admitted by all to be true Vertebrata.

coe

coe

coe'

FIG. 427.— Longitudinal frontal sections tli rough two embryos of DoUdioglo

in order to illustrate the development of the body-cavities. (After Davis.)
A, through younger embryo— the proboscis eorlom is arising as an anterior .•vn-iiiation of t.hr gut.
B, through older embryo— the collar coelom and trunk coelom arc arising by tln> transverse division of
posterior-directed tongues of the anterior coelom. cw-l, the proboscis coelom ; <•,„•-'. (]„• collar coclom ;
coe'i, tin' trunk coelom.

The development of Balanoglossus and Dolichoglossus is, however,
calculated to throw light on the previous history of the common'
stock of Vertebrata and Enteropneusta ; it takes us, as Lankester
has well said, into prechordal times. It will be noted that the
description of the development of Dolichoglossus, given by Bateson,
is confirmed in all important points by the description of the
development of Balanoglossus as given by Heider and Morgan;
we may therefore take it as being thoroughly well established!
Spengel's criticisms (1894) of Bateson's results, based on his own
observations on Tornaria larvae, made many years ago by methods
which are now superseded, are no longer valid, as he himself would
be the first to admit.

xvii PEOTOCHORDATA 585

We may therefore note that the Tornaria larva bears, in many
respects, a strong resemblance to the Bipinnaria larva of Asteroidea,
and, in external appearance, to the Auricularia larva of Holothuroidea;
from both of which it differs principally in possessing the posterior
ciliated band and the well-developed apical plate. The apical plate,
however, turns up in the Crinoid larva and in the late Echinnpluteus
larva, and it was probably once a feature of all Echinoderm
larvae. The tendency for the longitudinal ciliated band to rearrange
itself in transverse ciliated bands is exemplified by the late Echino-
pluteus larva, by the "Pupa" of Holothuroidea, and by the Crinoid
larva. The posterior ciliated baud of the Tornaria larva may be
the result of such a rearrangement. We arrive, finally, at the con-
clusion that no important difference divides the Tornaria from the
Echiuoderm type of larva ; the great difference between the two lies
in the nature of their metamorphoses.

It follows that Echinodermata and Enteropneusta (and through
the latter the whole of the Vertebrata) are descended from the
same stock of simple free-swimming animals. In this ancestral
stock the coelom was already divided into three sections on each
side, such as become delimited in the coeloni of the Echinoderm
larva as growth proceeds; and the middle sections, called
hydrocoeles in Echinodermata, and collar-cavities in Enteropneusta,
were produced into ciliated tentacles.

The main stem of the common stock which, in its day, must
have constituted a dominant type of animal, kept to the sea and
gave rise to the higher Vertebrata ; one division of which, the Pisces,
still dominate that element. An offshoot, which was destined to
give rise to both Echinodermata and Enteropneusta, dropped to the
bottom and took to gliding over the soft ooze. Certain of these
gliders finally fixed themselves to the substratum by the prae-oral
lobe, and gave rise to the Echinodermata ; whilst others degenerated
into burrowing habits and became Balanoglossida. But still others
seem to have learned to fix themselves by the ventral integument,
and thus gave rise to the other division of Enteropneusta known as
the Cephalodiscida. In these last, as. in the Echinodermata, the
middle or collar body -cavities are prolonged into ciliated tentacles ;
in fact, the great difference between them and the Echinodermata
(apart from the part of the body with which they fix themselves)
is that in the Cephalodiscida both collar-cavities are equally developed,
whereas in Echinodermata the left overpowers the right, and leads
to that peculiar ring-shaped growth of the left hydrocoele which
later imposes a radial symmetry on the primitive bilateral symmetry.
It is quite conceivable that Brachiopoda also, as indicated by the
three segments of their larva, may be distantly related to the same
type, but the substantiation of this suggestion would require a
great deal of further work.

If the reasoning outlined above be sound, a most interesting
conclusion can be drawn as to the origin of the peculiar Vertebrate

586 INVERTEBEATA CHAP.

nervous system, which differs so profoundly from the central
nervous systems of most invertebrates. The central nervous system
of Vertebrata must have been originally only a local intensification
of the general plexus of nerve fibres underlying the skin, which
exists both in Echinodermata and Enteropneusta. Its original
function was probably to act as a co-ordinating centre for the
activities of the tentacles of the two hydrocoeles. The importance
which it acquired in this way was retained when these tentacles
were lost, and it became the dominating nervous centre for all the

organs of the animal.

CEPHALOCHORDA

The Cephalochorda consist of a number of closely-allied species
of sand-inhabiting animals which are found in the tropical and
warmer temperate regions of the world. They have thus much the
same distribution as the Balanoglossida, but whereas these latter
live in soft black mud the Cephalochorda inhabit clean gravelly
sand.

Most of the species are referred to the genus Amphioxus
(BranchiostomcC). These animals, as is well known, possess the
general form of fish, and their muscles are arranged as in fish, in
series of blocks called myotomes. They possess a long tubular
spinal cord, underlaid by an indubitable notochord which
stretches from end to end of the body, whence the name Cephalo-
chorda. The pharynx is pierced by numerous long, narrow gill-
slits.

No one has ever questioned the relationship of these animals
with the vertebrata. If, therefore, we can discover in their develop-
ment, features which ally them with the Enteropneusta, the question
of the relationship of this latter group with the Vertebrata will be
settled in the affirmative.

The mode of development of the eggs of Amphioxus was first
discovered by Kowalevsky (1867-1877), and was more fully eluci-
dated by Hatschek (1881), whose account has been incorporated in
the text-books. The validity of this account was challenged by
Lwoff (1894), who has been followed by other workers. We our-
selves criticized Lwoff (1898), but our account has in turn been
challenged by Cerfontaine (1907), who supports a modification of
Lwoff's view, and by Legros (1907). A final answer to Cerfon-
taiue was given by us in 1909. The i'acts bearing on the controversy
will be given in the following pages.

Cerfontaine has given the best account of the segmentation of
the egg. He points out that the nucleus of the egg of Amphioxus is
nearer one pole of the egg than another, and that between this
nearer pole and the nucleus no yolk-granules are developed. On
this ground he asserts that the egg is not really alecithal, but
telolecithal, and regards this circumstance as a proof that the
ancestors of Amphioxus, like other Vertebrates, once had large

xvii PEOTOCHOEDATA 587

yolky eggs. But this idea is open to serious criticism. In all
alecithal eggs, even in those of Balanoglossus, the nucleus approaches
one pole of the egg when it undergoes division in order to form the
first polar body.

The first polar body in the case of Amphioxus is formed after the
egg is shed from the ovary into the surrounding coelonric space,
which is termed the gonocoele. From the gonocoele the eggs escape
through two slit-like openings into the atrial cavity, along which they
pass back to escape by the atrial pore into the sea. In the sea they
are fertilized by the spermatozoa which are emitted by the male.
Both eggs and sperm are obtained simply by collecting specimens of
male and female Amphioxus and placing them in jars of clean sea-
water. They spawn usually in the evening about 6 P.M. The
spermatozoon enters the egg by the pole which is farthest from the
nucleus, and only after this happens is the second polar body given
off. After this the egg secretes a vitelline membrane, inside which,
accordingly, the second polar body is enclosed, and this body remains
visible during the earlier part of the development and is used by
Cerfontaine as a landmark. The vitelline membrane is formed as in
the egg of Echinus, by the coalescence of a row of spherical drops
emitted from the egg, the outer walls of which coalese to form a
coherent skin. The spermatozoon travels upwards through the egg
to meet the egg-nucleus, which descends to meet it. The compound
zygote-nucleus is, therefore, nearer the centre of the egg than was the
nucleus of the unfertilized egg, and it is surrounded on all sides by
yolk-granules as in any other typically alecithal egg.

The fertilized egg begins at once to segment, and it is easy to
keep the developing eggs in jars of clean sea-water, in which they
will live until the larvae hatch out about ten hours after fertiliza-
tion. These larvae live for a day or more until they have developed
a mouth and one gill-slit, further than this stage it has not been found
possible to rear them in captivity. Later stages are procured by
fishing in the water with a tow-net. The experiment, however, of
feeding these larvae on diatoms has never been tried : it is extremely
likely that an attempt to do this would be crowned with success.

The eggs, in their earlier stages of development, are best preserved
in the mixture of solution of corrosive sublimate and glacial acetic
acid ; but once the larvae have hatched, indeed once the gastrulation
is over, osmic acid is the best preservative. It is necessary to impreg-
nate them thoroughly with this reagent, in order to stiffen their delicate
tissues and to prevent their collapsing in the process of dehydration.
Also it is absolutely necessary to embed first in celloidin, and then in
paraffin, if good results are to be obtained. The minute size of the
embryos renders it possible to obtain what is equivalent to a good whole
mount, by immersing the fragment of celloidin in cedar oil. The posi-
tion of the embryo in the celloidin block can, in this way, be accur-
ately ascertained, and so the difficult question of orientation is solved.

The egg divides in the usual way into two and then four blasto-

588 INVEETEBKATA CHAP.

meres. Of these four, two, which later are shown to be anterior, are
rather smaller than the others, so that even at this early period the
egg is bilaterally segmented. These four blastomeres in turn divide
into an upper and a lower tier, and so the 8-cell stage is attained ;
but the four upper cells, termed by Cerfontaine micromeres, are
rather smaller than the four lower cells termed macromeres. There
are therefore two larger and two smaller micromeres, and two larger
and two smaller macromeres.

In attaining the 16-cell stage each cell divides into right and
left daughters by radial planes, so that two tiers of eight cells
should be formed; but four macromeres move downward and four
micromeres upwards, so that four tiers of four cells each are formed.
Each cell then divides into upper and lower halves, and in the

FK; 4-2S. — Stages in the segmentation of the egg of Amphioxus lanceolatus.

(After Cerfontaine. )

A, 3-J-i-rll stage seen from the side. B, optical sagit I al sect i. m of a yonng blastula. an.p,
animal pole of the egg; pi2, second polar body ; wg.p, vegetative pole of the egg.

32-cell stage we have actually eight tiers of four cells each. But,
as is shown in Fig. 428, this unstable arrangement does not persist.
The blastomeres glide on one another, and we get a circle of four cells
at both the animal and the vegetative pole, and three intervening
tiers of eight cells each. The tier at the animal pole consists of the
smallest cells, that at the vegetative pole of the largest, and in the
intermediate tiers we have a gradual passage from the one size to
the other.

At the next period of cleavage the planes of division are no
longer parallel to one another in all the cells. The equatorial cells
divide into right and left daughters, but the planes of division in the
polar cells are oblique. After the next cleavage the egg has divided
into 128 cells, and these commence to flatten out against each other
and to take on the character of a columnar epithelium which is
ciliated.

At the next stage, when there are 256 cells, the embryo is a

XVII

PROTOCHOKDATA 589

spherical blastula. At this stage, if we compare the blastula to a
school globe, and the animal pole to the North pole, and if we
imagine a traveller passing from the North pole to the South, he
would continually encounter larger cells ; whilst if he passed round
the equator from a point which we may compare to Africa, to a point
which we may compare to South America, he would also pass from
smaller to larger cells — since the two anterior blastomeres of the
4 -cell stage, and all the cells descended from them, are smaller
than the two posterior blastomeres and their descendants.

In the next stage the blastula flattens on one side and becomes
hemispherical (Fig. 429, A). On the flat side there are the largest
cells, which are now of a tall columnar shape. At one edge of the
flat surface there is an abrupt passage from cells of this character to
comparatively small cells, but at the other edge the tall columnar
cells pass gradually into the lower cells which form the hemispherical
wall of the blastula. The first edge of the flat surface we may term
x, the second y.

The process of gastrulation begins within an inflection of the
flat surface near the edge named x (Fig. 429, B). The invagination
is therefore not a symmetrical invagination of the centre of the
lower surface, as in Balanoglossida and Echinodermata, but is such as
to give the impression of its being due to the push of an invisible
finder directed against the flat surface near the edge x.

o o

This asymmetry in the invagination was not noticed by
Kowalevsky and Hatschek, but was first noted by Lwoff, and is
made by him the foundation stone of his theory. According to him
the invagiuation occurs in two stages : in the first, the columnar
cells, which according to him alone represent the endoderm, are
invaginated. Following this stage, however, small cells are inflected
at the dorsal lip of the blastopore, and these Lwoff regards as
ectoderm. These small cells form eventually the roof of the archen-
teron, and from them notochord and mesoderm are developed, and these
structures therefore, on this theory, would be of ectodermal origin.
With this view Cerfontaine (1907) substantially agrees, except that
he maintains that, at a later stage in gastrulatiou, ectoderm is in-
vaginated round the ventral lip of the blastopore as well as round the
dorsal lip.

Now, it will be observed that Lwotf's case stands or falls with the
presumption that, in the hemispherical stage of the blastula, ectoderm
and endoderm are already finally separated from one another. If
this presumption is ill-founded the whole procedure of splitting the
process of gastrulatiou into two stages is condemned. A careful
examination of the hemispherical blastula proves that, except at the
edge x, there is no such sharp delimitation of the columnar cells
which make up the supposed endoderm, from the supposed ectoderm,
as Lwoff postulates. The delimitation at x is seen to be due to the
presence there of a zone of rapidly dividing cells, and it is plausible
to associate the invagination itself with the pressure exerted by the

590

INVEETEBEATA

CHAP.

masses of new cells formed. Indeed, in all cases where the process of
gastrulation has been carefully investigated, as for instance in the
egg of Echinus, invagination is preceded by a rapid multiplication of
cells, near the spot on the wall of the blastula which is invaginated.

' '^l$£%i$^;*-f1'

•* * • "•"••»• »'*•••** • *\"*i •» *vV -<-A

FIG. 429. — Stages in the gastrulation of the egg of Amphioxus lanceolatus.
All the figures represent median sagittal sections.

A, stage of hat-shaped blastula. B, the imagination of the eniloderm well advanced; notr the
Miundi'il cells at the dorsal lip of the lilastnpore. C, the ^astnila has grown in length— tin- neural ]ilate
is clearly marked. D, the upgrowth of the ventral lip of the blastnpure has liegiin. n.p, neural jilale ;
X, dorsal lip of the blastopore ; Y, ventral lip of the blastopore.

There is no ground, however, for assuming an inflection of cells round
the dorsal lip of the blastopore, indeed, as invagination proceeds we
obtain definite evidence that this is not the case. For although at
first the nuclei of all the cells of the embryo are alike, being large,
clear, and vesicular, with relatively little chromatin, yet soon the

xvn PROTOCHORDATA 591

nuclei of the cells of the outer layer become more dense and stain
with avidity (Fig. 429, B).

This phenomenon appears to be the outward sign of a physio-
logical differentiation between the ectoderm and endodermal cells;
and all the invaginated cells, those which were columnar on the flat
surface of the hemispherical blastula, and also those which are sub-
sequently invaginated and form the roof of the archenteron, retain
clear and vesicular nuclei, and differ from the ectodermal cells in this
respect. Further, the rapidly dividing cells at the edge x, which, in
consequence of the contraction following on completed karyokiuesis,
are small and rounded, are of two kinds ; those which are destined to
be added to the ectoderm have deeply staining nuclei, those which are
destined to be added to endoderm have vesicular nuclei. Here, then,
we have proof that at the edge x we have a meristem like that of
a plant, i.e. a growing zone, from the cells produced by which, different
layers are differentiated.

The processes which we have been describing lead to the formation
of a cup-shaped gastrula with a huge blastopore. As Morgan and
Hagen (1900) have shown, there is a general growth in length of the
embryo, due to divisions of cells scattered throughout both ectoderm
and endoderm. In virtue of this growth the cup becomes more
comparable to a thimble.

The rudiment of the first definite organ now appears. This is
the neural plate (n.p, Fig. 429), the so-called " medullary plate,"
which here, as in all the higher Vertebrata, is the first organ to
appear. The ectoderm cells on one surface of the thimble become
more columnar than the rest, and this surface becomes slightly
flattened, and so the neural plate is formed. The appearance of the
neural plate settles definitely the question as to whether edge x corre-
sponds to the dorsal edge of the blastopore or not. It also proves
that the diameter of the blastopore and the long axis of the nerve
plate are at right angles to one another.

The wide blastopore becomes then reduced to a narrow pore by a
new process of growth, which starts at the lower lip of the blastopore,
in the region corresponding to the lower limit of the flat surface in
the hat-shaped blastula, a region which we have already denominated //.
Here a meristem of dividing cells is formed, exactly like that which,
in a previous stage, existed at the edge x. By the activity of this
second zone an up-growth of the lower ventral lip of the blastopore
takes place, and all that is left of the blastopore is a small rounded
aperture near the dorsal surface. Fig. 430 is intended to show how
much of the endoderm and ectoderm of the gastrula is developed
from the walls of the hat-shaped blastula, and how much owes its
origin to the two zones of growth, x and //. The blastopore is closed
by the meeting in the middle line ol two lateral folds of ectoderm
cells termed the neural folds (n.f, Fig. 431). These flaps originate
at the sides of the blastopore and extend forwards along the sides of
the neural plate. They meet first over the blastopore and last over

592

INVERTEBBATA

CHAP.

= '--

cS
bD

o
O

P<
O

the front end of the nerve plate. Here, indeed, for a considerable time
an aperture persists — the so-called neuropore. It follows that, at the
hinder end of the animal, a short vertical canal, covered over by the

neural folds, leads upwards from the
archeuteric cavity to the canal of the
nerve chord. This is the so-called
neurenteric canal (n.e, Fig. 431, D).
In a later stage of development
the anus opens at the lower end
of this canal. The anus may be re-
garded, consequently, as a remnant of
the lower edge of the blastopore, and
indeed in the Urodela this portion of
the blastopore never closes, but re-
mains permanently open as the anus.
As soon as the blastopore is closed,
the formation of the notochord and
of the coelom takes place. The
notochord originates from the mid-
dorsal region of the archenterou.
Here a strip of cells, in which the
yolk - granules have disappeared,
becomes folded up into an arch (ch,
Figs. 431, 432), which becomes cut
off from the rest of the endoderm
as a tube with a minute cavity.
This cavity speedily vanishes and the
notochord thus becomes a solid rod of
cells. The radial arrangement of the
cells in the rod soon becomes lost, i.e.
the cells no longer meet in a point,
but inter digitate with one another.

The coelom arises as two pairs
of evaginatious of the dorso-lateral
walls of the gut. The front pair
might be described as a pair of
pockets, the hinder, more correctly,
as a pair of longitudinal coelomic
grooves, the front ends of which
overlap the pockets. The front pairs
we shall compare to the collar-
coelomic cavities (col.coe, Fig. 431) of
the Enteropneusta, the hinder pair to
the trunk-coelomic cavities of those
animals. The walls of these
coelomic sacs constitute the mesoderm. After the neural plate is
covered over by the meeting of the neural folds, it becomes bent
into the form of a U (Fig. 432), a,n.d. finally, by the meeting of

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XVII

PKOTOCHOKDATA

593

the edges of this, into a tube which is the neural tube <>r spinal
cord. During the larval life of the animal this tube opens in front
by the neuropore (n.p.o, Fig. 436, B).

Soon after the formation of mesoderm an extremely rapid growth
in length of the embryo sets in, then hatching takes place, and the

eft

trcoe

FIG. 431. — Transverse sections through an embryo of Amphioxus lanceulatva just after
the completion of gastrulation, in order to illustrate the development of nerve cord,
notochord, and coelorn.

A, section through the anterior region of the embryo, showing- the neural plate exposed and the
evaginations of the gut, which give rise to collar and trunk coelomic cavities. B, si'ctiuii through a
more posterior region of the embryo, showing the neural folds nearly meeting above the neural plate,
and the arching of the miil-dcirsal section of the gut to form the notochord. C, section through the
hinder end of the embryo, showing the anal diverticuluin and tin- union of the neural folds. I), sect ion
behind the last, showing the neurriiti-ric canal. «.</, anal diveiticulum ; <-li . rudiment of I he notorhord ;
col.coe, rudiment of the collar coelom ; K.I-, nem enteric canal ; «./, neural folds; ».//, neural plate ; tr.coe,
rudiment of trunk coelDin.

minute larva swims around by the aid of the cilia which clothe the
whole ectoderm. The growth in length is chiefly localized in the
hinder region of the embryo, and includes the hinder ends of the
trunk-cavities, so that these grow iii length pari passu with the rest
of the larva. There is, however, a general growth in length of all
VOL. i 2 Q

594

INVEETEBEATA

CHAP.

np

parts of the larva, as evinced by the fact that the diameter decreases,
up till the end of the second day ; and the constituent cells of all the
tissues become smaller in transverse section. The left anterior

coelomic pocket, or collar-
cavity, retains an open
connection with the arch-
enteron for a considerable
time, and the hinder ends
of the trunk-cavities also
remain open to the arch-
enteron for a considerable
time, whilst their anterior
portions are grooved off
from it.

These anterior parts
become divided into
segments which are called
somites (som, Fig. 432).
The first pair of somites
are formed from the collar-
cavities. The somites are
at first small spherical
vesicles situated at the
dorso-lateral angles of the
gut. They have at first
only minute cavities. They
soon begin to grow down-
ward between gut and
ectoderm, and the cells
forming their walls become,
for the most part, thin
and flattened. An excep-
tion to this statement is
constituted by the cells
forming the inner walls of
the somites, where these
walls abut on the noto-
chord. These cells remain
columnar in cross-section,
and develop fibrils in their
cytoplasm, and so form
the longitudinal muscles
of the larva.

When five or six
somites have been formed,
that portion of the arch-
enteron which lies in front of the anterior pockets, or collar-cavities,
becomes grooved off from the rest, and simultaneously divided

FIG. 432. — Transverse sections through an older
embryo of Amphioxus lanceolatus than that
represented in the previous figure, to show the
further development of nerve cord, notochord, and
coelom.

A, anterior section, showing on the left the first somite
cut off from the front end of the trunk coelom, on the right
the collar-cavity. B, posterior section, showing the open
groove in which the trunk coelom terminates posteriorly, ch,
rudiment of notochord; col.coe, collar coelom; »./, neural
fold ; n.p, neural plate ; som, somite ; tr.coe, trunk coelom.

XVII

PROTOCHOEDATA

595

into right and left cavities, of which the right is larger than the left.
These are the so-called head-cavities, which we have compared to the
proboscis-cavity of Enteropneusta. The remainder of the archenteron
now constitutes the gut.

Meanwhile the somites derived from the trunk-cavities become
divided into upper portions, termed myotomes, from whose inner
walls the muscles are formed, and lower portions, which fuse with
their predecessors and successors to form the general body -cavity or
splanchnocoele. The right and left splanchnocoeles meet with one
another and fuse into one cavity in the mid-ventral line beneath
the gut. Above the gut they remain separate from one another, and

Lcotl

rcott

arch

Fid. 433. — Illustrating the formation .and development of the head-cavities of

..-I mphloxu& lanceolutus.

A, transverse section through the anterior region of a larva with six myotomes— the head-cavities are
seen to be developing as outgrowths of the front end of the gut (archenteron). B, transverse section
through the anterior region of a larva two days old .just before the mouth opens— the left head-cavity is
a thick-walled vesicle ; the right head-cavity is a thin-walled vesicle and lies beneath the left one. arch,
archenteron (gut) ; eli, notochord ; e.c, vacuolation of ectoderm where the external opening of the left
head-cavity will be formed later ; l.ivll, left collar-cavity ; l.h, left head-cavity ; n.t, nerve tube ; r.cull,
right collar-cavity ; r.li, right head-cavity.

between them lies a blastocoele space, double in front but single
behind, which is the rudiment of the dorsal aorta.

Since new somites are being continually cut off from the hinder
parts of the trunk-cavities, all stages in the development of a somite
may be made out in one and the same individual. The somites derived
from the collar -cavities, however, do not become subdivided like the
rest, nor do they fuse with the splanchnocoeles. In early larval life, at
any rate, these lower parts constitute cavities lying at the ventro-
lateral regions of the animal, outside the splanchnocoeles, whilst the
upper portions of the collar -cavities, above the myotome region,
extend forwards at the sides of the nerve cord. The general form of

196

INVERTEBEATA

CHAP.

the collar -cavities, as seen from the side, is therefore that of a
reversed S-

The next changes which occur are, the enlargement of the front
end of the gut as the rudiment of a pharynx, and the formation of
the mouth. The mouth appears on the left side of the animal; the
pharyngeal wall adheres at this spot to the ectoderm and a perforation
takes place (m, Fig. 435). Soon after this the left head-cavity, which
is small and spherical and lined with columnar cells, fuses with the
ectoderm and acquires an opening to the exterior ; whilst the right
one becomes thin-walled, and extends to the extreme anterior end of
the larva beneath the notochord (Fig. 433, B). It is known henceforth
as Hatschek's pit.

The first gill-slit is formed in the mid-ventral line by the union
of a dbwngrowth of the pharynx with an ectoderrnal ingrowth.

Simultaneously a structure
nf called the club-shaped gland
makes its appearance. This
arises as a pocket, high up
on the right wall of the
pharynx opposite the mouth.
This pocket curves down-
ward and forward, and opens
to the exterior below and in
front of the mouth. Below
the opening of the club-
shaped gland the wall of the
pharynx becomes modified
to form a V-shaped ridge,
with the apex of the V
pointing inwards. The ridge
consists of glandular cells
it is the rudiment of the

col.coe

trcoe

FIG. 434. — Diagram of longitudinal sagittal sec-
tion of Amphioxus lanccolatus to one side of
the middle line, in order to show the mutual
relationships of head, collar, and trunk cavities.

col.coe, collar coelomic pouch ; It.. me, head coelomic
pouch ; n.e, neurenteric canal ; •»./, neural fold ; «./>,
neural plate ; tr.coe, trunk coelomic pouch.

and of cells carrying short cilia, and

endostyle of the adult (en<lst, Figs. 436, 437, 439, 441).

This extraordinary larva, which now possesses mouth and anus,
and is able to feed itself, leads an active swimming life for about
three months. During this period new somites are added behind,
and new gill-slits appear in a single series behind the first ; but they
are no longer mid-ventral, but are actually situated on the right side
of the larva. The development of these has been worked out by
Lankester and Willey (1890), who term them primary gill-slits.
As many as fourteen (according to Goodrich [1910] fifteen) of these
primary gill-slits are formed.

The hinder ends of the coelomic grooves or trunk-cavities have
by this time become solid and have finally separated from the gut ;
the neurenteric canal also has become a solid string of cells, and this,
and the neighbouring tissues, give rise to a growing zone, the tail-
bud. From this bud there grows out a post-anal extension of nerve
cord, notochord, and myotomes, known as the tail (Fig. 437).

PEOTOCHOEDATA

597

The tail is a most characteristic organ of the Yertebrata. It is
true that the name " tail " is often loosely applied to the posterior

Icoll

rcoll

cl.gl.ex

gs.end

n.t

FIG. 43fi. — Illustrating the mutual relationships of collar-cavities anil splanchnocoeles

in Amphio.i'iis lanceolatits.

A, transverse section ] Kissing, just in front of tin- mouth of;t larva, in which thei ulli and lirst ^ill-
slit have been formed— the collar-cavities lie at the sides of the pharynx. B, transverse section through
the region of tin- lirst ^ill-slit of a larva in which the month has not. yet. tieen formed— the .splanchno-
coeles appear piessing the collar-cavities down wan Is towards the ventro-lateral angles of the pharynx ;
the gill-slit is seen to be formed by the meeting of ectodermal and endodenual outgrowths. C, trans-
verse section through the hinder end of the pharynx of a larva in which the month and first gill-lit
have been formed ; the collar-cavities have disappeared, c/i, notochon! ; cl.gl.ex, external opening of the
club-shaped gland; <M-<'''', <j.x.cwl, ectodermal and endodermal rudiments of gill-slil resjii'ci ivel.v ; l.coll,
left collar-cavity ; l.*i'l, left. s])lanchnocoele ; m, front lip of month ; my.c, niyocoele ; //./, uei \e I ube .
/•.CM//, i JLjht collar-cavity ; r.xtil, riglit s]]]anchnocoele.

part of the body of any animal, if it happens to be thin and flexible,
but its proper application is to a post-anal extension of the body

598 INVERTEBRATA CHAP.

formed as a secondary outgrowth from a posterior zone of growth.

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In many fish the tail is several times longer than the body, and it is
characteristic of the low place which Ampliioxus occupies in the

XVII

PKOTOCHOKDATA

599

vertebrate phylum as compared with
tish that its tail-growth is insignificant.

In older larvae a slight ectodermic
thickening along the line of the posterior
extension of the first somite, on the
right side, is observable ; this thicken-
ing is the first rudiment of the atrial
fold, which overhangs the gill -slits.
A similar fold is developed on the left
side at a later period of development,
and during the metamorphosis into
the adult form these two folds unite
beneath the ventral surface of the
animal and enclose the atrial cavity.

Hollow outgrowths from the inner
walls of the myotomes give rise to
tubes which insinuate themselves
between the myotomes on the one hand
and notochord and nerve cord on the
other (Hatschek, 1888). These are
the lower sclerotomes (scl'2, Fig!
438) ; from their inner walls a fibrous
sheath is developed which enswathes
notochord and nerve cord. Their
outer walls furnish a sheath, or fascia,
for the muscular fibres of the myo-
tomes.

From the uppermost angles of the
myotomes similar outgrowths arise
which we may term the upper sclero-
tomes (scl1, Fig. 438), and become com-
pletely cut off from the myotomes. Thus
they give rise to a series of pockets lined
by coelomic cells which are termed the
fin-ray cavities. These cavities were
described by Hatschek (1888) ; their
origin from the myocoele was first seen
by G-oldschmidt (1905). The cavities
are arranged in a single series in the
mid-dorsal line, four or five occupying
a space corresponding to the breadth
of a myotome. They appear to be
formed by outgrowths arising alter-
nately from the myotomes on the right
and left side. The ventral wall of
each becomes thickened and forms
the gelatinous peg known as the
fin-ray.

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600

INVEETEBEATA

CHAP.

During the larval life the excretory organs are formed. These
are true nephridia comparable to those of Oligochaeta, Nemer tinea,
and Platyhelminthes. They consist of tubes ending internally in
tufts of solenocytes or flame cells. Their origin has been described
by Goodrich (1909). When they are first discernible they consist of
small pear-shaped masses of cells, almost certainly ectodermal in
origin, situated at the lower borders of the primitive gill-slits. They
rapidly become hollow and long solenocytes grow out from their
inner ends. These solenocytes extend up the left side of the body

s-.ii/

FIG. 438. — Diagrammatic traiisver.su sections through the hinder region of two young
specimens of Amphloxus hinrcnlntiiK, in order to show the origin of the selerotomes.
(Alter Hatschek, slightly altered.)

A, through a larva with five primary gill-slits — the lower sclerotome is just beginning to be formed.
B, through a specimen just after the metamorphosis — the lower sclerotome has extended upwards be-
tween the myutnme .•mil the notochord, and the upper sclernlome lias given rise to the tin-ray c.-ivily.
fit, notncliord ; ('.", dorsal aorta; rny.c, myocoele ; ii.r, nerve curd ; »•/!, upper sclerotome; w/-, Inwer
selriutume ; u'n septum dividing myocoele from splauchuocnele ; s.i.v, suli-iiite.stiual vein ; xjil, splaueh-
nocoele ; r.J'.r.i; ventral fin-ray cavity.

to the level of the dorsal aorta (-so/, Fig. 439). In the adult the
solenocytes are much shorter than in the larva. One very large
nephridium lies in the forward extension of the right collar-cavity,
and opens behind into the mouth. This is called Hatschek's
nephridium.

As the larva grows older it seeks lower and lower levels in the water.
Finally, after about three months of larval life, the metamorphosis
sets in, and during this period the larva frequently lies on its side on
the bottom. Before metamorphosis begins, however, the rudiments
of the genital organs make their appearance. Their development
lias been elucidated by Boveri (1892). They arise as small buds of
cells (germ, Fig. 440), which sprout from the anterior lower angles of

XVII

PKOTOCHOEDATA

601

the myotomes, and which project into spaces derived from the posterior
lower angles of the myocoeles, as the cavities of the myotomes are

« r "2 E — &

called. These spaces form the gonocoeles of the adult: they soon
become cut off from the myocoeles from which they are, derived l>y
the growth of septa, and each gonad projects into the gonocoele
derived from the myocoele in front of the one to which it belongs.

t.musc

gon.c

t.musc

FK;. 440. — Illustrating the development of the genital organs of Amphioxus lanceolntus.

( After Boveri. )

A, a portion of the body-wall of a young Amiiliio.rti.i, 9 millimeters long, viewed as a transpaient
object, in order to show the relation of the genital rudiment to the myotomes. B, a small port ion nl a
similar preparation from a still younger specimen, in order to show the origin of the germ cells. (', a
small portion ol' a similar preparation from a slightly older specimen than that from which li is taken,
In slio\v the indentation of the wall of the myotome by the genital rudiment. I"), a small portion of a
similar preparation from a specimen 14 millimeters long to show the formation of the gonocnele from
the myocoele. K, a. portion of a transverse section through a specimen of the same size as that from
which' I) is taken. </'•'''«', primitive germ cells ; i/an, rudiment of genital organ ; i/ox.r, gonocoele ; mil,
myotome; /».</.<•, myocoele; scl2, lower sclevotome ; sri>t, septum, dividing gonocoele I'rom myocoele ;
Linn*-, transverse muscle in the floor of the a trial cavity.

602

CHAP. XVII

TEOTOCHORDATA

603

The changes which occur during metamorphosis have been
described in detail by Willey (1891). The first gill-slit and the

•f— *~: \. •§ - \- x — -^- ** *"** - ""^Jyjtrfi^-ip %• p=t^ ^_^^£j^j/-'- jT-j''

p.g.s<

FIG. 441. — Illustrating the metamorphosis of the larva of „ /////<// iu.>-n?: lanceolatus.

(After Willey.)

A, larva, with full number of primary gill-slits, seen from the right side ; six thickenings of (lie
pharyngeal wall above the primary gill-slits indicate the beginnings of the secondary gill-slits ; the
atriiil folds are not yet united. B, larva in which the hindermost primary gill-slits have disappeared ;
six secondaryigill-slits have been formed and the atrial folds are united ; viewed from the right side.
C, larva in which eight secondary gill-slits have been formed, live of which are divided by tongue-bars ;
the primary gill-slits have been reduced to nine, and tongue-liars have begun to be formed in them ;
the endostyle has been shifted to the mid-ventral line, and oral cirri an- beginning to be formed ;
viewed from the ventral side, nt, atrial cavity ; at.f, atrial fold ; ti.r, buccal cavity ; b.i; brain-vesicle ;
i-li, notochord ; cl.ijl, club-shaped gland; en, endst, endostyle; /./•.'-, tin-ray cavities; l.h.c, left liead-
cavifcy ; m, border of mouth ; M.p, Mtiller's papillae; m.yi./, niefapleural fold; ».<•, nerve con I ; //./,

neural tube; nc, eye-spot;

•"

'-, •;>.;(.«'•*, the first, second, eleventh, twelfth,

and fourteenth primary gill-slit, s ; />///, pigment sjmts in nerve cord ; .-•.(/..<',

Ihe liist and

secondary gill-slits ; slum, stomodai'Uin ; '.''. tongue-bai ; c," vcliini : /'•.», wheel-organ.

club-shaped gland disappear simultaneously. Sc\'cra,l of the more
posterior of the "primary" gill-slits also disappear, and in this way

604 INVERTEBRATA CHAP.

the number of these is reduced to eight. A new series of eight gill-
slits make their appearance on the right side of the larva, above the
primitive gill-slits. These new gill-slits (termed by Willey the
secondary gill-slits) grow downwards, pressing the primitive gill-
slits back to the mid-ventral line of the larva, and eventually on to
its left side. Thus the "primary" gill-slits form the adult gill-
slits of the left side, and the " secondary " gill-slits those of the
right side. In this way the lower borders of the primary gill-slits
become the dorsal borders, and the excretory organs reach the
position in which they are found in the adult, vix. the dorsal border
of each gill-slit.

At the same time, in both primary and secondary gill-slits, septa
grow out from their dorsal edges, extend across them, and eventually
divide each of them into two. These septa are the tongue-bars (t!b,
Fig. 441). The endostyle, which like the gill-slits lay originally on
the right side of the pharynx, is forced downwards to the mid-ventral
line ; it grows backwards until it extends along the whole length of
the pharynx. The buccal cavity or stomodaeum is formed by the
outgrowth of two cheek-like folds from the collar region (region of
the first myotome), which extend forwards beneath the notochord. and
enclose between them a space which formerly was part of the external
world, lying in front of the larval mouth. The larval mouth persists
at the bottom of the stomodaeum as an opening in the so-called velum,
leading into the pharynx.

On the dorsal surface of the buccal cavity an extensive series of
ciliated grooves makes its appearance. These grooves radiate from
the opening of the left head-cavity, now termed Hatschek's pit, and
their function seems to be to carry off the secretion of this pit. They
are termed collectively the wheel-organ (-w.o, Fig. 441). At the
side of the buccal cavity the ciliated rods, known as oral cirri, grow
out (Fig. 441, C). The atrial ridges unite to form the floor of the
atrial cavity ; on their inner surfaces ectodermic thickenings appear
which are believed to be excretory in function, and are termed
Miiller's papillae (Fig. 441, B).

The metamorphosis may now be regarded as complete, and the
animal takes up its habitat in a vertical burrow in the sand. In this
burrow it leads a sedentary life, only occasionally emerging from it
to make a rapid dash through the water and then seek a new burrow.

The young Amphioxus has still to produce new gill-slits, since, it
has only eight pairs to start with ; and it has only the rudiment of a
liver. As the animal increases in size, new gill-slits gradually
appear behind the existing gill-slits on each side, and a full-grown
specimen may have as many as 100 pairs. Each gill-slit begins as a
simple perforation which is then bisected by the growth of a tongue-
bar. The liver begins as a little ventral pouch of the gut immediately
behind the pharynx. This pouch grows forward and becomes pushed
up on to the right side of the animal. Eventually it becomes so long
that its tip reaches nearly to the velum.

xvii PKOTOCHORDATA 605

THE AFFINITIES OF AMPHIOXUS WITH THE ENTEROPNEUSTA

We have now to endeavour to answer two questions, viz. («) Does
the developmental history of Amphioxus, as we have sketched it,
afford support to the idea that the Enteropneusta have vertebrate
affinities; and (&) How are we to explain the extraordinary asym-
metrical larva, which nevertheless becomes metamorphosed into an
adult which is nearly bilaterally symmetrical ?

With regard to the first question, it must be remembered that
even if Enteropneusta be admitted to the Vertebrate phylum, they
must, nevertheless, be widely separated from Cephalochorda. Between
a tirade of structure in which the neural tube was confined to the
collar region, and in which the notochord is represented by a small
anterior diverticulum of the pharynx destined to support the base of
the proboscis region ; and a grade of structure in which neural tube
and notochord extend throughout the entire length of the body, an
enormous gap intervenes, to span which an enormous lapse of time
must have been required.

Nevertheless, in the segmentation of the egg, and in the forma-
tion of the layers, there is a fundamental agreement between
Enteropneusta and Cephalochorda. The segmentation of the egg of
Doliclioglossus, as sketched by Davis, appears to be of the same general
type as that of the egg of Amphioxus. The same hemispherical
blastula stage is found in Ampliioxus and in Balanoglossus, as de-
scribed by Heider ; and in both cases the archenterou is large and
nearly fills the blastocoele, and the embryo, immediately after
gastrulation, grows markedly in length. In both cases too (if we
follow Morgan [1891] in his account of the development of the New
England Tornaria larva), the mesoderni arises from the archenteric
wallas five outgrowths, viz. an anterior unpaired pouch and two pairs
of lateral pouches. In both the neural plate arises in the same way, as
do also the protecting flaps of ectoderm which cover it in. In both
it is eventually converted into a neural tube. In both the left division
of the anterior coelomic pouch opens to the exterior by a pore. When
we add to these resemblances the anatomical similarities between
the adult forms in respect of notochord, gill-slits, and tongue-bars, it
will be admitted that a very strong case for the vertebrate affinities
of the Enteropneusta has been made out. We have not to reconstruct
a single organ, and we take as our starting-point a very simple free-
swimming animal represented by the Tornaria larva.

On any other theory of the origin of Vertebrata, such as the idea
that they came from Annelida, a new mouth has to be manufactured
and other radical changes in function have to be postulated, for
which there is no precedent in the evolutionary changes which we
can determine with moderate certainty.

From the conclusion that the Enteropneusta are Vertebrata, some
very interesting consequences follow. The proboscis-cavity of the
Enteropneusta is represented by the " head-cavities " of Amphioxus,

606 INVEKTEBRATA CHAP.

as we have seen, and by the premandibular cavities of higher
vertebrates, from the walls of which most of the eye muscles arise.
Now in the Tornaria larva we find at the apex of the proboscis an
apical plate of nervous and sensory cells on which two eye-cups are
situated ; and in the embryos of the frog the optic areas can be
recognized as pigmented spots in the region of the fore-brain whilst
this is still an open plate.

It appears probable, therefore, that the ectoderm covering the
proboscis of the Enteropneusta corresponds to the fore-brain of
Vertebrata, whilst the collar region of the Enteropneusta corresponds
to the region of the mid-brain of Vertebrata and what lies beneath it,
viz. the mandibular cavities, from the walls of which jaw muscles
and the superior oblique muscles of the eyes arise. The mandibular
cavity would then correspond to the collar-cavity of Enteropneusta
and to the region of the first myotome in Amphioxus. How far the
ventral extension of the first myotome, which is so clear and distinct
from the splanchnocoele in the early larva of Amphioxus, corre-
sponds to the system of cavities in the lips of the adult, called by
Van Wijhe (1901) collectively the stomocoele, is a matter requiring
further investigation.

The connective tissues and peritoneal membranes of the larvae of
Amphioxus are difficult to preserve and stain, only mixtures con-
taining osniic acid seem to confer on them the power of taking up
stains so as to Vie clearly distinguishable. The slit-like coelomic
cavities are apt to collapse, and then it is impossible to be sure of
their extension and limits, as their adherent walls look like single
membranes. The best results are obtained by staining the sections,
after preliminary stain in bulk with haematoxylin or eosin, with
a 1 per cent aqueous solution of picronigrosin.

But the working out of the larval development under con-
ditions like these is still a task for the future. If we assume that
the lip-cavities of the adult Amphioxus arise from portions of the
collar-cavities of the embryo, and that the collar-cavities are homo-
logous structures in Amphioxus and Euteropneusta, then we may
note that the ciliated oral cirri, which aid Amphioxus in obtaining
its food, are outgrowths of the lip-cavities. These cirri may then,
perhaps, be compared to the ciliated tentacles which grow out from
the collar-cavities in Cephalodiscida, and to the radial canals, and
the tube feet, which are branches of these canals, in Echinodermata.
These canals and their 1 tranches are outgrowths of the left hydrocoele,
which we may compare to the left collar -cavity of Amphioxus and
Enteropneusta.

When we endeavour to answer the second of our two questions
we must admit that the larvae of AmpJiioxus are so extraordinary as
to present a serious problem for those who, like ourselves, believe
that the larval stage represents, in however modified form, an ancestral
condition of affairs. Balfour considered them so abnormal that, when
they were first described by Kowalevsky, he thought they must be

xvii PKOTOCHOEDATA 607

pathological. That a bilaterally symmetrical embryo should pass
through an asymmetrical pelagic larval stage, in order to attain the
form of a practically symmetrical burrowing adult, seems to be in
complete contrariety to what we should expect.

But a very plausible solution has been suggested by Stafford
(quoted in MacBride, 1909). He points out that the ancestor of
AmpMoxus could not have suddenly jumped from a pelagic to a
burrowing existence. Some intermediate condition of life must have
existed. What was the intermediate state of affairs ? In the case of
other animals which have deserted a pelagic for a more humble form
of existence, we have reason to believe that a habit of gliding over
the surface of the mud preceded a burrowing life. But a vertically
flattened animal like AmpJiioxus could not do this and keep on an
even keel. The moment it ceased swimming it must have tended to
fall on one side. This circumstance can actually be observed in the
older larvae of Amphioscus. Let us assume, therefore, that the ancestors
of Amphioxus, after deserting their free-swimming life, passed through
a stage when they lay on their left sides on the bottom. Under these
circumstances it would be an advantage to twist the mouth round to
the left side, so as to bring it near the detritus which served as food,
and to twist both sets of gill-slits round to the upper right side, so
that the waste water might be ejected without disturbing the sub-
stratum on which the animal was feeding. Similar conditions of life
have led the modern flat-fish to become asymmetrical, they have
twisted the mouth down and the two eyes round to the upper side of
the body.

But if this solution sounds plausible two further questions may
be asked, viz. («) Why does only one row of gill-slits develop ? and
(&) Why does the asymmetry appear at that stage of its development
when, to judge from its environment, the larva ought to be bilaterally
symmetrical ?

The answer to the first question has an important bearing on the
way in which ancestral adult organs are represented in the larva.
The larva in almost every case (see Chap. I.) has been much reduced
in size in comparison with the ancestor which it represents. If larval
organs were reduced 011 the same scale as the whole animal they
might be reduced to dimensions which would render their functions
difficult, if not impossible of performance. Too narrow gill-slits, for
instance, might become useless owing to the viscosity of water in
passing through small apertures. Hence arises a tendency, which we
have noted elsewhere, to sacrifice number to size; thus, of the two series
of gill-slits which the ancestor undoubtedly possessed, only one is
developed in the 'larva in order that the individual slits may have
room to spread. The missing gill-slits are held over, so to speak, till
adult habits are about to be taken up.

That a left-sided mouth and asymmetrical gill-slits should appear
in a free-swimming larva is only another example of an exceedingly
widespread phenomenon, viz. the reflection of features belonging to

608 INVERTEBEATA CHAP

later stages of development into earlier stages of ontogeny. This
phenomenon, termed heterochrony by Lankester, which meets the
comparative embryologist at every step of the road on which he
travels, is one for which no adequate explanation has as yet been
suggested, but it seems to us that it is of the utmost interest in
weighing theories of heredity and of the origin of variation.

In conclusion, therefore, we maintain that the asymmetries of the
larva of Amphioxus are due to the existence of a former " Hat-fish "
condition, but that these asymmetries have been reflected backwards
into a previous free-swimming condition so as to appear in the
pelagic larva.

We have now placed lief ore the reader the arguments, which
seem to us convincing, that the Enteropneusta are related to the
vertebrate phylum. As we have already stated, however, all zoologists
are not in accord with this view. We have not here discussed the
objections which have been raised to it, because, in the second volume
of this work, the reader will have an opportunity of learning at
first hand the arguments on the other side, and will then be best
able to weigh both sides of the case for himself.

UEOCHORDA

The group of Urochorda, more familiarly known as Tunicata,
comprises animals, the vast majority of which are sessile, and many
of which have much the same external appearance as sponges. By
the older zoologists they were classed, with Polyzoa, as Molluscoida.
It never entered into the imagination of any one that they had
affinities with the Vertebrata till Kowalevsky (1867) showed that the
larva possessed a notochord, a tubular dorsal nerve cord expanding in
front into a brain-vesicle, and a pair of gill-slits. The larva has a long
post-anal tail to which the notochord is confined, and on this account
the name Urochorda (ovpd, a tail) is given to the group. Since a
brain-vesicle has been developed at the anterior end of the spinal
cord, and since there is a tail, we are driven to conclude that the
Urochorda must have branched off from the Vertebrate stem when
the Vertebrate stock had evolved far beyond the level represented
by the Cephalochorda ; for in this latter group there is a mere
rudiment of a brain-vesicle, and the tail is only beginning.

The Urochorda include a few minute forms termed Larvacea,
which retain tail, notochord, neural tube, and brain-vesicle throughout
life, and remain free-swimming. About the development of these
animals little or nothing is known. There is also a small group
termed the Thaliacea which has secondarily acquired free-swimming
habits; the larval tail and notochord are lost in the adult, but the
sphincter muscles, which in ordinary forms surround mouth and
anus, are developed into hoop-like bands, and by the peristaltic action
of these muscles progression is effected.

The vast majority of Urochorda, termed the Ascidiacea, are

xvii PKOTOCHOEDATA 609

sessile forms which increase by budding. In one small sub-group,
the Ascidiae luciae, the colony has become free-swimming; in
another sub:group, the Ascidiae simplices, the power of budding
has apparently never been acquired. If we compare the larvae of the
rest of the Ascidiacea, termed the Ascidiae compositae, with the
larvae of the Ascidiae simplices, we find that the former are dis-
tinguished from the latter by the precocious appearance of the
peculiar features of the adult. In other words, the Ascidiae simplices
preserve the larval stage in its most unmodified form, and it is to
them, therefore, that we turn in order to select a type for special
description.

CYNTHIA

The most recent work on the subject is by Couklin (1905), who
lias followed the development of Cynthia partita, cell for cell, until
the attainment of the larval form. He has done the same for Ciona
intestinalis, and for Phallusia (1911), and his researches have made
it probable that the same general scheme applies to all the Ascidiae
simplices. What is related for Cynthia will hold true, with slight
modifications, for the common simple Ascidiaiis on the coasts of
England, and the work of Van Beneden and Julin (1884) makes it
clear that the development of Clavdina, the simplest form of the
Ascidiae compositae, follows the same general course, although, even
here, the .telescoping of development, characteristic of compound
Ascidians, has begun to appear.

Cynthia partita is an Ascidian found in abundance at Wood's
Hole. It lives fairly well in laboratory tanks, and it lays eggs in
the evening, which, in the course of about ten hours, develop into
fully organized free-swimming larvae. In order, therefore, to be able
to study the development by daylight, Conklin extracted eggs from
the ovary and artificially fertilized them in the morning. Of such
artificially fertilized eggs few developed, but these few were sufficient
to enable the development to be thoroughly investigated. In the
case of Ciona intestinalis, on the contrary, it is quite easy to artificially
fertilize the eggs if the sperm from another individual be used. The
animal's own sperm will not fertilize its eggs.

The eggs of Cynthia were examined living, on a slide, in sea-water,
covered with a coverslip supported by fragments of coverslip about
i mm. thick. Under these circumstances the eggs could be rolled
about and examined from all sides. When it was desired to make
whole mounts, Kleinenberg's picro-sulphuric acid gave the best results.
The best method of staining was to use both Delafield's haematoxylin
and picric acid. The eggs are first stained with haematoxylin, and
this is differentiated in the usual way by adding acid alcohol ; then
for dehydration the alcohols of 90 per cent and absolute strength,
made yellow by the addition of picric acid crystals, are used. In this
way the mass of the egg is stained yellow, but the nuclei are stained
blue. For sections it was found best to preserve the eggs in picro-acetic

VOL. i 2 H

610

JNVEETEBEATA

CHAP.

'.m

cr

FIG. 442. — The egg of Cynthia partita
before and during fertilization.
(After Conklin.)

[The yellow cytoplasm is indicated by
dotting the dark-blue cytoplasm by dark
shading.]

A, egg In-torn fertilization with large
germinal vesicle. B, egg immediately after
fertilization, showing the down-streaming
of the yellow cytoplasm and the outflow of
the contents of the germinal vesicle. C,
egg a little later, showing the aggregation
of the yellow cytoplasm to form the yellow
crescent at the posterior side of the egg.
ec.t.cy, clear cytoplasm which will give rise
to ectoderm; e.in, egg - membrane ; g.v,
germinal vesicle ; t.c, test cells ; y.cr, yellow
crescent.

acid. Such material can lie stained
with haematoxylin followed by eosin
dissolved in oil of cloves, on the slide.

Conkliu commenced his study of
the development with the ovarian egg.
In the young oocyte there is no yolk,
and the nucleus occupies a nearly
central position in the egg. On the
one side of the nucleus is a rounded
mass which stains deeply with rosin.
This Conklin considers to be the
" attraction sphere," which functioned
in the cell division which gave rise
to the oocyte ; it now functions as
yolk -nucleus, i.e. the deposition of
yolk -granules takes place round it
as a centre. A layer of peripheral
cytoplasm remains free from yolk ; in
this, however, yellow pigment granules
are deposited. The yolk spherules are
of a slaty-grey colour. There is an
enormous vesicular nucleus (germinal
vesicle), with a large nucleolus, and
near the nuclear membrane a few
chromatiii granules.

As the oocyte grows it is surrounded
by the so-called test cells. These are
simply follicle cells or rudimentary
ova ; round the nucleus of each there
is the same collection of yellow
granules as are found in the peripheral
layer of the ovum. These " test cells "
become actually embedded in the
peripheral layer of the oocyte whilst
it is growing, but when it is ripe and
discharged from the ovary the test
cells are expelled from the cytoplasm,
and a chorion is formed. Between
the chorion and the egg there is a
space formed by the shrinkage of the
latter, the perivitelline space. In this
the expelled test cells lie.

After laying, the egg begins to
undergo maturation changes. The
nuclear membrane dissolves and so
does the large nucleolus. The clear
nuclear sap flows upwards and forms
a cap of clear cytoplasm, lying at

xvii PROTOCHORDATA 611

what will be the animal pole of the egg. In the centre of this cap
lie the chromosomes which are connected together by a faintly
granular substance. Out of this granular substance the first matura-
tion spindle is developed, the spindle fibres appearing as rods of
granules. No further development takes place unless the egg be
fertilized.

The spermatozoon is able to burrow through the chorion ; it
enters the cytoplasm at the vegetative pole of the egg, as in the case
of the egg of Amphioxus. Immediately after its entry the division
initiated by the maturation spindle is completed, and the first polar
body is given off. This consists of clear cytoplasm and does not
divide. A new spindle is reconstructed out of the remains of the
old one, and a new division occurs by which the second polar body is
given off. The second polar body is in all respects similar to the
first ; both 1 todies remain attached to the egg, in many cases through-
out the whole of the embryonic development, and so the position of
the animal pole can be accurately determined. In neither matura-
tion division is there a trace of a centrosome.

Whilst the maturation divisions have been proceeding, cytoplasmic
movements of a violent character have been taking place. Both the
clear cytoplasm and the clear peripheral layer with the yellow
granules flow downwards to the vegetable pole of the egg, and form
a cap there which surrounds the sperm head. With such violence
does this flow take place that the " test cells " are often carried along
with it, and are found aggregated in a heap at the vegetable pole
(Fig. 442, B). At the animal pole is left only a small mass of clear
substance surrounding the maturation spindle. The slaty yolk is
now massed at the animal pole. At the vegetable pole the clear
protoplasm is superficial to and. more extensive than the yellow
substance.

The spermatozoon at first moves towards the centre of the egg
from whatever point it enters, until it has traversed the clear and the
yellow protoplasm and reached the yolk. This is its penetration
path. Then it changes its direction and moves towards the posterior
end of the egg. This is its copulation path. As it thus moves it
seems to draw with it a large part of the yellow protoplasm, which
forms a crescent just below the equator of the egg, with the two
arms reaching half-way round ; the centre of this crescent is the lower
pole of the egg. The clear cytoplasm moves towards the posterior side
of the egg, around and outside the yellow substance (Fig. 442, C).

The male and female pronuclei meet near the lower pole of
the egg ; since the female pronucleus, after giving off the second
polar body, descends to meet the male. The zygote nucleus then
moves inwards towards the egg's centre. The male pronucleus,
before uniting with the female pronucleus, has developed at out-
side a well-marked aster. Before the zygote-nucleus divides, this
aster divides into two parts, placed one at each end of the first
spindle ; so that, although in the maturation divisions no asters are

612

INVEETEBEATA

CHAP.

found, in all the divisions which occur during the development of the
egg asters are formed. As the zygote-nucleus moves inwards it
draws with it the clear cytoplasm, leaving most of the yellow cyto-
plasm behind. Some clear cytoplasm, however, is left at the surface
as a narrow band above the yellow crescent, and some yellow
cytoplasm moves inwards. The egg is now ready to undergo the
first cleavage.

ectcy

B

cr

y.cr

D

chn

y,cr

mes

FIG. 443. —Stages in the segmentation of the egg of Cynthia partita. (After Conklin.)
[The different coloured cytoplasms are indicated as in the preceding figure.]

A, 2-cell stage viewed from behind. B, S-cell stage viewed from the vegetative pole. C, 16-cell
stage viewed from the vegetative pole. D, segmenting egg passing into the 32-cell stage, viewed
from the vegetative pole, fh.n, chorda-neural cells; ect, ectodermal cells; ect.cy, cytoplasm which
will give rise to the ectoderm ; mes, mesodermal cell ; p.b, polar bodies ; r.j>, vegetative pole ; ,'/.'•<,
yellow crescent.

The first cleavage divides the egg into two precisely equal cells ;
the yellow crescent is also divided into two equal parts, and into each
crescent, after division, an intrusion of grey yolk takes place, which
indents it (Fig. 443, A). The two sides of the indentation join round
the intrusion, and the crescent is thus re-established. In this way
the yellow substance receives accessions from the yolk. After
division the nuclei, with the clear substance surrounding them, rotate

xvii PKOTOCHOKDATA 613

round the egg towards the animal pole. The yolk is thus displaced
from this pole, which, although it was temporarily the seat of the
most of the yolk, remains ever afterwards relatively free from yolk
and hecouies the seat of an accumulation of clear cytoplasm ; although
even here a thin external layer of cytoplasm, with yellow yolk-
grains, is found.

At the next cleavage the two cells become four ; the two anterior
cells are slightly larger than the two posterior, which receive all the
yellow sul istance. The four cells then become eight in the usual
way, by dividing into two tiers, and the four cells at the animal pole
are smaller than the four at the vegetable and contain all the clear
cytoplasm. There is a cross furrow observable when eggs in this
stage are viewed from the side. This arises from the circumstance
that the furrows separating upper and lower cells come to slant
downwards and forwards, and consequently they strike the vertical
furrow dividing anterior from posterior cells in different places.
The anterior vegetative cells are the largest, and the anterior animal
cells the smallest in the egg.

We may here anticipate the final result of the development so
far as to say, that the animal pole of the egg corresponds roughly
to the antero-veutral region of the embryo, whilst the vegetative
pole corresponds to the postero-dorsal region of the embryo. If the
reader confuses " animal " and " dorsal " regions of the egg, it will
be impossible to follow the account intelligently.

When the next cleavage occurs the spindles of all the dividing
nuclei are parallel to the horizontal plane, but are oblique to the
vertical plane of the egg. The 16-cell stage (Fig. 443, C) consists
of two tiers of eight ceils. The animal hemisphere, in consequence
of the direction of the spindles of the dividing cells, is narrow in
front and broad behind, whereas the vegetative hemisphere is broad
in front and narrow behind, and here the two smallest cells in the
egg are, delimited; these consist almost entirely of yellow substance
and constitute a valuable landmark. The two cells immediately in
front of these contain the rest of the yellow substance, but in
addition a great deal of yolk. The remaining four of the vegetative
cells contain principally the slaty-blue yolk, but have a certain
amount of clear substance near their anterior borders.

The next cleavage period raises the number of cells to thirty-two.
On the vegetative side of the egg the purely yellow cells divide so
as to form four, lying side by side. The half-yellow, half-blue cells
divide so as to separate the yellow and Uue 2>ortions ; and the yellow
portions lie to the outside, so that there is now a crescent, concave
in front, of six yellow cells, running across this hemisphere! The
anterior, wholly blue cells, of the vegetative hemisphere, divide into
anterior and posterior daughters ; the anterior daughters lying lower
than their sisters. There result two crescents of four cells each,
the front one lying just beneath the equator of the egg, and the
posterior running across the middle of the back. The cells of the

614 INYERTEBRATA CHAP.

posterior crescent contain only slaty -blue, yolky substance, but those
of the anterior crescent contain a rim of clear substance in front and
slaty-blue behind. The cells of the animal region of the egg, corre-
sponding to the ventral hemisphere of the embryo, divide into
similar daughters, all alike ; in front, however, the two most anterior
just surmount the equator. They all consist of clear substance and
yolky material, hut the clear substance is much more prominent
than the yolk. At this stage, too, they are all columnar, and the
cells of the vegetative pole broad and flat; at a later period, as we
shall see, the shapes of the cells of the two poles become interchanged.
The cells have separated from one another internally so as to give rise
to a blastocoele, and the egg has now become a blastula (Fig. 445, A).

It is now possible to see clearly the exact regions of the embryo.
The cells of the animal hemisphere, or antero-ventral portion of the
embryo, give rise to ectoderm. Those two, however, which surmount
the equator in front when the egg is viewed from the dorsal aspect,
i.e. from the vegetative side, give rise to the anterior portion of the
neural plate. The blue cells of the vegetative hemisphere give rise
to the endoderm, but the most anterior cells of this hemisphere,
consisting of clear and blue substances, form the dorsal lip of the
blastopore, corresponding to the edge x in Amphioxus. They are
called chorda-neural cells (cli.n, Fig. 443, D) by Conklin, because,
like the cells forming that edge in the embryo of Amphioxus, they
give rise by further division to both neural plate cells (ectoderm) and
notochordal cells (endoderm^), the former being constituted by the clear
and the latter by the blue portions of the cells. The transverse 1 >and
of yellow cells gives rise not only to the longitudinal muscles of
the tail of the larva but also to what Conklin calls "mesenchyme,"
i.e. anterior mesoderm to which the muscles and genital organs of
the adult owe their origin.

A register of the whole thirty -two cells shows, therefore, fourteen
ventral ectoderm cells, two neural plate cells, four chorda-neural cells,
six eudoderui cells, and six yellow mesoderm cells. The blue cells
form a broad band in front which gives rise to the pharynx of the
larva, and to a tongue, projecting backwards between the horns of the
yellow crescent, which is the rudiment of the tail endoderm.

By the next cleavage sixty-four cells are produced. Turning-
first to the animal hemisphere, we find that the spindles of the
dividing cells are directed in various ways, but the result is to
produce a coherent sheet of twenty-eight similar ectoderm cells.
The neural cells divide so as to produce a curved transverse line
of four cells, and to the outer edges of this crescent there is added,
on either side, a cell from the rest of the ectoderm which also con-
tributes to the formation of the nervous system ; so that, in this
way, a crescent of six neural cells is formed.

Coming now to the vegetative hemisphere, we find that the chorda-
neural cells have divided into anterior and posterior daughters.
The four anterior are also neural cells and enter into the formation

XVII

PEOTOCHOEDATA

615

of the. neural plate. The four posterior are the rudiment of
the notochord (Fig. 444, A). The blue endoderm cells divide chiefly
into anterior and posterior cells, but in front the lateral endoderm
cell on either side divides into an inner and an outer daughter cell.
The outer cell on either side contains less yolk than the inner,
and is the so-called anterior mesenchyme cell, which is the rudi-
ment of the most anterior part of the mesoderm.

Of the six yellow cells, the two outer ones on either side divide
into dorsal and ventral components. The dorsal component con-
tains less yellow substance, than the ventral, and appears of a paler
colour and gives rise to mesenchyme. The inner cell on each side
divides into anterior and posterior daughters ; the anterior daughters
with the ventral daughters of the outer cells form the rudiment of

ch

®

amch

mch

pmch

Fie. 444.— Illustrating the gastrulation of the egg of Cynilna partita. (After Conklin.)

[Tim coloured cytoplasms are indicated as in tin- two previous figures.]
Both figures represent eggs viewed from the vegetative pole, i.e. from above and behind.

A, stage in which the semicircular dorsal lip of the blastopore is just beginning to form. B, stage in
which the invagination of the endoderm is well advanced, n.mch, anterior meseiichyme cell ; cli, noto-
chordal cells ; nn-li, mesenchyme cells ; »./>, neural plate cells ; ji.iiicJi, posterior mesenchyme cell. The
dotted cells which are not mesenchyme are mesodermal cells.

the longitudinal muscles of the tail of the larva, while the posterior
daughters of these inner cells form mesenchyme and constitute the
posterior mesenchyme cell on each side. The divisions of the cells
of the vegetative hemisphere take place first, and these cells pass into
a state of rest, during which they alter their form and become columnar,
whilst the cells of the animal hemisphere are dividing. These latter,
on the contrary, now cease to Ite columnar and become flat (Fig. 445).

If we make a register of the whole sixty-four cells, we find :
animal hemisphere, twenty-six ordinary ectoderm cells, six neural
cells ; vegetative hemisphere, four neural cells, four notochordal cells,
two anterior mesenchyme cells, four mesenchyme cells, two posterior
rneseuchyme cells, six muscle cells, and ten endoderm cells.

After this cleavage we can no longer speak of a general period
of cleavage affecting all the cells of the egg, because one set of cells

616

INVERTEBKATA

CHAP.

will have passed iiito a new period of cleavage before another set
have completed the previous cleavage. The crescents of cells, neural
and notochordal, derived from the posterior lip of the blastopore, increase
to eight cells each. The two front muscle cells on each side are in-
creased to four, whilst the mesenchyme cells above them also divide.

The gastrulation now begins, as in Amphioxus, by an inwardly
directed cytotaxis of the endoderm cells. The beginning of this
is no doubt really the change in shape that, as we have just noted,
the cells of the vegetative hemisphere have undergone, namely, from
a flat to a columnar shape. This change leads to a contraction of
their surface area, whilst the contrary change in shape undergone
by the ectoderm cells increases their area.

At this stage in the proceedings there is, in front, a semicircular
arc, opening backwards, of eight chordal cells; and behind a semi-

ect

end

end'

end

FIG. 445. — Sections through eggs of Cynthia partita, in order to illustrate the changes in
form undergone by ectodernial and endodermal cells during the process of gastrula-
tion. (After Coiiklin.)

Tlic small circles in the cells represent yolk-grannies.

A, transverse section through egg vith about forty cells, showing columnar ectoderm and quadrate
endoderm. B, longitudinal sagittal section through egg with sixty-four cells, showing endoderm and
ectoderm cells both columnar. 0, longitudinal sagittal section through egg with one hundred and ten
cells, showing flattened ectoderm cells and columnar endoderm cells, a-t, ectoderm cells ; iml. endo-
derm cells.

circular arc, opening forwards, of twelve mesenchyme cells. These
two arcs taken together form a complete circle inside which are the
endoderm cells. Beneath the mesenchymal arc lies an arc of six
muscle cells, whilst outside the chordal arc is an arc of eight neural
cells. If, however, as Castle (1894) maintains, the first cell of the
mesenchymal arc on each side enters into the formation of the
notochord, then the circle described above will consist of ten noto-
chordal cells in front and of ten mesenchymal cells ] >ehind.

At a stage a little older than that shown in Fig. 444, B, the
neural arc described above begins to grow back, overarching the
chordal arc and the endoderm cells. Soon afterwards the ectoderm
cells lying outside the mesenchyme ring increase in number and
become involved in this overarching process. It follows that whereas
the outline of the lip of the gastrula, viewed from the vegetative sur-

XVII

PEOTOCHOEDATA

617

face, appears semicircular, the blastopore is really wide in front and
narrow behind ; for behind it is a groove between the two columns
of muscle and mesenchyme cells on each side, the mesenchyme cells
being above and external as regards the muscle cells.

The overarching rim of cells, which is the anterior lip of the
blastopore and corresponds to the region marked x in the gastrula

tnch

•sup

FIG. 446. — Illustrating the closure of the blastopore in the gastrula of t'l/ntt/in /m,-titn.

(After Conkliu.)

A, dorsal view of advanced gastrula, showing the blast opore as a minute pore at- (In1 hinder end of
tin- neural plate. 13, posterior view of advanced gastrnla, showing the neural folds. C, lateral view of
advanced gastrnla, showing the rotation of the mesodennal lands into a vertical posit ion liy the up-
growth of the ventral lip of the blastopore and the division of the inesenchynie into a superior and an
inferior mass, blji, disappearing blastopore ; iiicli.i/if, interim- mass of inesenchynie ; HH//.M//S superior
mass of mesenchyme ; ma, mesodennal band; ii.f, neural fold ; n.ji, neural plate.

of Amphioxus, continues its growth backward till it covers three-
quarters of the dorsal face of the embryo. Then the groove between
the lateral walls of muscle and mesenchyme becomes tilted upwards
till it becomes vertical, and the mesenchyme cells are placed in
front of the muscle cells. This change is due to the sudden up-
growth of the posterior and ventral lip of the blastopore, the region
corresponding to the region // in the gastrula of Amphioxus. The

618

INVERTEBRATA

CHAP.

blastopore, instead of being directed posteriorly, becomes directed
dorsally (Fig. 447) ; in fact, the change which occurs is precisely

met

mch

FIG. 447. — Optical sagittal section of gastrula of Cytilliin jim-tita. (After Conklin.)

l,lji, hla-itoporr ; r//, notochord ; inch, mesenchyme ; ms, iiii-sodcnnal band in vertical position ;

n.p, neural plate ; pit, pharynx.

parallel to the change which
takes place during the closure
of the blastopore in Amphioxus.

The column of mesenchyme
cells then becomes broken into
two masses, an anterior one adher-
ing to the top of the column of
muscle cells, and a posterior one
attached to the foot of this column.
Soon afterwards the vertical
columns of muscle cells are again
forced into a horizontal position,
and eventually constitute two rows
of muscle cells, one above the
other, on each side of the embryo.
Each row consists of about six
cells, and each cell forms a long,
horizontal lozenge-shaped struc-
ture, and develops muscular fibrils
in its substance. This change,
from a vertical to a horizontal
position, which occurs in the
muscle cells, is due to the growth
in length of the hinder end of
the embryo, a process which leads
anterior mesenchyme is now situated
11s, and is incorporated in the trunk

FIG. 448. — Dorsal view of an embryo of
t'l/nl.hin jiai-tittt. after the closure of the
1 ilastopore, in order to show the formation
of the tail. (After Conklin.)

itirli, nirsfiichyme which will nivc rise to the
niHSodfrm of the adult Ascidiun ; m-s nn-so-
dernud hand drawn out into a horizontal position
by tin- growth of the tail ; «./, neural folds ; n.p,
neural plate.

to the formation of the tail. The
in front of the rows of muscle ct

XVII

PKOTOCHOKDATA

619

o£lhe embryo (Fig. 448) ; it lies on each side of the pharyngeal wall,
wedged in between this and the ectoderm (Fig. 449). The posterior
mesenchyme is situated at the hinder end of the tail (Fig. 450).

When the hlastopore has heen reduced to a pore on the dorsal
surface, the neural folds (often termed the medullary folds) make
their appearance (n.f, Fig. 446). These are a pair of folds of
ectoderm arising from the sides of the neural plate, meeting each
Other in the middle line behind the blastopore, but diverging from
one another widely in front. As development proceeds they inert
each other in the middle line farther and farther forward ; thus
the blastopore is covered in, and, as in Amphioxm, a neurenteric
canal is formed. Then the neural plate is covered in and converted
into a neural tube covered by
ectoderm.

The neural plate is wide
in front and gives rise to a
correspondingly wide section
of the neural tube ; this is the
brain-vesicle ; the remainder
of the neural tube is narrow
and constitutes the spinal
cord. For a short time the
front part of the brain-vesicle
communicates with the exterior
by a pore termed the neuro-
pore, corresponding to the
neuropore of the larva of
AmphioxUS, and, like it, due FIG. 449. — Transverse section through the middle

ph.

mch

of a gastrula of Cynthia
Conklin. )

(After

nii-li. mi'sriifliymi' lying at tin- sides <>(' the gut ; n.f.
neural fold ; n.]>, neural plate ; ////, cavity of pharynx.

to an imperfect union of the
neural folds in front. The
neuropore, however, soon closes
(Willey, 1893), but reopens
at the close of larval life when the larva undergoes metamorphosis.

The larva soon afterwards bursts its choriou and enters on its
free-swimming career, propelling itself like a fish by lateral blows of
its tail. For a complete exposition of its organisation (which is
taken for granted by Conklin) we must turn to the older work of
Kowalevsky (1866, 1871), who worked chiefly with Cionn intestinalis
and with Phallusia mam millitt/i.

In the fully developed larva a mouth is formed by a small
iusinking of the ectoderm in front of the nerve tube. This insinking
involves the spot where the ueuropore was situated, so that the
brain- vesicle would open into the pharynx if the neuropore were
still open. This is the case in Clavelina (Willey, 1893), but in
simple Ascidians, as we have seen, the neuropore becomes closed
during free-swimming life, but reopens during metamorphosis. The
hinder end of the endoderm forms a solid cord underlying the noto-
chord ; it soon breaks up into wandering cells. On the dorse-lateral

620

INVERTEBRATA

CHAP.

surfaces of the trunk a pair of imaginations make their appearance.
These are the atrial invaginations ; they meet and fuse each with
two evaginations of the pharynx, and thus are formed the first two
pairs of gill-slits, which, for reasons to be given later, we designate
as gill-slit No. 1 and gill-slit No. 4.

From the hinder wall of the pharynx there grows out a tube-
like diverticulum, the rudiment of the adult intestine. The end
of this curves up the left side of the body, and in the larvae of some
species even comes into contact with the ectoderm, not far from the
mid-dorsal line ; but no anus is formed till the free-swimming life is

tend

u.e

FIG. 450. — Longitudinal sagittal section of tadpole of Gynthia partita just before it
escapes from the egg-membrane. (After Conklin.)

/(.)>, brain-vesicle ; c/i, uotochord ; MS, mesodermal land (seen by slight obliquity of the posterior end
of the section); n.t, nerve tube; pJi, pharynx ; t'.eml, ventral cord of endoderm cells in the tail.

over. Along the ventral wall of the pharynx there is differentiated
a broad strip of columnar cells ; this is the endostyle.

Finally, the wall of the brain-vesicle undergoes modification. On
the right side a hemispherical outgrowth takes place, and the cavity
of this cup becomes filled up with a secretion which becomes
pigmented. This is the cerebral eye of the Ascidian tadpole, and
corresponds, without doubt, to one of the two optic vesicles of the
brain of a higher Vertebrate. Close behind the eye rudiment there
is another pigmented area of epithelium which is the rudiment of
the ear or balancing organ. It is soon separated from the eye and
forced round to the floor of the brain-vesicle by an expansion of the
epithelium between it and the eye, which thus gives rise to the thin-
walled epithelium forming the greater part of the wall of the brain-
vesicle. The ear eventually forms a median prominence, shaped like

XVII

PKOTOCHOEDATA

621

I

a '

'.r.

o s

'S V

•e
g

2 "f
"o >

•« i.

v-. o

^ o

a a

C3 c"

I
§

a

Six

endst

FIG. 452. — Anterior portion of
free-swimming tadpole of
the simple Ascidian Phal-
lusia maiiii/iillata, seen from
above. (After Kowalevsky. )

u, position where anus \vill In-
formed ; at, atrial involutions ;
6.y, brain-vesicle ; emlxt, i-ndosl \ l^ ;
fx, fixing processes ; i/.<i, ygi, the
first two gill-slits ; /'«/, intestine;
in, mouth; inn, t-hin (mental pro-
cess); ms, longitudinal muscles nt
the tail; n.t, nerve tube; oc, eye-
cup; fit, otolith ; /ill. phai-ynx.

622 mVERTEBKATA CHAP, xvn

a cup on a stalk, carrying in its apex a spherical pigmented concre-
tion, the otolith. The hinder wall of the brain-vesicle is thick, and forms
a ganglion, termed the visceral ganglion (gang.visc, Fig. 454, F).
There is a protuberant region which we may term the chin (run, Fig.
451). Below the. mouth the ectoderm develops three papillae of
glandular cells, one median and two lateral, which are the organs of
fixation.

Although the larva has a mouth it cannot feed, because this is
closed by a gelatinous cuticle termed the test or mantle. The test
is secreted by the ectoderm and enswathes the whole body, covering
over both mouth and atrial openings. It contains certain cells called
test cells, which are budded from the ectoderm (t.c, Fig. 451), but
these cells are to be carefully distinguished from the cells bearing
the same name which surround the egg ; these latter, as we have
seen, are rudimentary ova.

After a short free life the larva fixes itself to the substratum by
the papillae on its chin, and then undergoes a rapid degenerative
metamorphosis. By the contraction of the ectoderm of the tail, the
notochord, nerve cord, and muscles are bent and broken into
fragments, which are rapidly devoured by wandering cells (Fig.
453). The ectoderm becomes invaginated so as to form pockets, and
these pieces of intucked ectoderm are attacked and devoured by
wandering cells ; and by these processes the whole of the tail is
disposed of. The chin region grows enormously, and by this growth
the mouth is carried upwards, away from the substratum to which
the animal is attached. This process is similar to the one by which
the mouth is rotated upwards in the metamorphosing larvae of Girri-
pedia, Polyzoa, Entoprocta, and Grinoidea ; and it occurs for the same
reason in all four cases, viz. from the physiological necessity of lifting
the mouth up so as to put it into a better position for catching
floating plankton.

Willey (1893) has followed in some detail the metamorphosis of
dona intestinalis, and his results have been confirmed by other
workers. He finds, as already mentioned, that when the metamor-
phosis begins the neuropore .is reopened ; and he suggests, what is
a 'priori extremely likely, that this opening has persisted, in a potential
form, as union of the ectodermic wall of the brain-vesicle with the
ectoderm all through the larval life. During larval life a gutter,
which we may term the hypophysial canal (h>yp, Fig. 454), is
formed in the dorsal wall of the brain-vesicle. This gutter becomes
completely grooved off from the vesicle behind, where it is continuous
with the cavity of the spinal cord, hut opens into the vesicle in front.

At the beginning of metamorphosis, when the neuropore is
reopened, the hypophysial canal becomes continuous with this pore,
and the rest of the brain -vesicle becomes completely grooved off from
the canal. The brain-vesicle then rapidly degenerates (Fig. 455),
and the sense-organs are broken up and absorbed. The adult
ganglion is formed as a new proliferation (Figs. 454, 455) from the

.

tail

Fiii. 453. — Illustrating the metamorphosis of the tadpole of <_'i\ni<i

(After Willey.)
A. young tadpole just after fixation, seen from the right side— the mouth is still in tin* lai \ai position

ami tlie tail is just beginning to degenerate. B, ymmg li\ei| dona, in which the month is rotated up-
wards and the 'tail is reduced toagranular mass. C. yomiff fixed Cifntn, in which the month ha,- at lained
the ni>per pole of the animal and in which the tail has disappeared. «, anus; at, atriul canal; li.r,
bruin-vesicle ; eiutst, endostyle ; ganrj.ad, adult ganglion ; f/.*1-*, the first four gill-slits ; hyp, hypophysial
canal ; int, intestine ; m, mouth ; mn, chin (mental process) ; n.c, nerve cord ; n.t, nerve tube ; oes,
oesophagus; pc, pericardial sac ; pph, peripharyngeal ciliated band; py.g, pyloric gland ; st, stomach.

623

624

INVERTEBEATA

CHAP.

dorsal wall of the hypophysial canal; the visceral ganglion of the
larva, which formed the thick posterior wall of the brain-vesicle,

FIG. 454. — Transverse sections through the brains of Ascidian tadpoles to illustrate the
development of the hypophysial tube and of the adult ganglion. (After Willey.)

A, B, sections through brain of a newly-hatched tadpole of Ciona intestinalis : A, the more anterior
section, shows the pigmented otolith and the hypophysial canal running in the wall of the brain-vesirli' ;
B, the more posterior sc-rtkm, shows the hypophysial canal opening into the brain-vesicle and tin- rup-
shaped support for the otolith. C, section through the brain of a just-fixed tadpole of Ciona intestinal if,
showing the degenerating larval brain and the hypophysial tube above it. D, section through the brain
of a young Ciona intestinalis, showing the adult ganglion as a new formation on the dorsal wall of the
hypophysial tube. E, F, sections through the brain of a tadpole of Clnrelinn /(•y»iJii/i)/-»/i.< : E, the
more anterior section, shows the brain-vesicle and the origin of the hypophysial tube and of the adult
ganglion from its wall ; F, the more posterior section, shows the cavities of the nerve tube and of the
hypophysial tube and the larva visceral ganglion. 6.i', brain-vesicle; gang. ad, rudiment of adult
ganglion; gang. vise, visceral ganglion; li>/p, hypophysial tube; n.t, nerve tube; oc, degenerating
remnant of the larval eye ; ot, otolith and its support.

XVII

PEOTOCHOEDATA

625

degenerates and disappears. The greater part of the spinal cord is lost
with the degeneration of the tail, but the small portion which remains
loses its cavity ; whilst 1'roin the posterior end of the hypophysial
canal glandular pockets are formed, which give rise to the sub-
neural gland of the adult, and which have been compared to the
pituitary body of the higher Vertebrate.

The intestine, which in Ciono is less developed in the free-
swimming larva than is the case in some other species of simple

gang ad

FIG. 455. — Longitudinal sagittal sections through the brain-vesicles and hypophysial
tubes of just-fixed tadpoles of Cionu intestinalis. (After Willey.)

A, earlier stage ; note that the hypophysial tube opens behind into the nerve tube. B, later stage.
b.r, degenerating larval brain-vesicle ; tjait'i.nil, adult, ganglion ; li/i/i, hypophysial tube ; n.t, nerve lube.

Ascidians, grows longer, and acquires an opening to the exterior
by fusing with the ectoderm near the mid-dorsal line. This opening
is the anus. The proximal portion of the intestine swells out to
form a globular sac which is termed the stomach. From the
stomach grows out a pouch, which, by rapid branching, gives rise
to a tubular gland called by Willey the pyloric gland. This gland,
whose branches enswathe the intestine (Fig. 453, C), almost certainly
corresponds to the liver of Ampliioxus.

A median groove, which involves the anus and both atrial
openings, is formed in the dorsal surface of the animal. The sides

VOL. I 2s

626 IN VERTEBE AT A CHAP.

of this groove meet each other, and in this way the atrial cavity
of the adult is formed. The larval test becomes detached from the
ectoderm covering most of the body, which it hereafter loosely
enswathes, and the mouth becomes open. The test, however, remains
attached to the body near the posterior end of the endostyle. Here
a process is formed which projects into the test, and from which
fresh test cells are budded off during life.

The pericardium arises during free-swimming life. The mode
of its development has been satisfactorily made out by Kiihn (1893),
who has summarized and corrected the accounts of earlier observers.
In the free-swimming larva a thickening of the ventral wall of the
pharynx can be observed (Fig. 456, A). This thickening is at first
a mere doubling of the cells forming the wall of the pharynx in this
region. At the close of larval life it becomes a round mass of cells
distinct from the pharyngeal wall. In this mass a cavity appears
which opens into the pharyngeal cavity (Fig. 456, B). This cavity is,
however, soon cut off from the pharynx, and forms the pericardia!
vesicle. Then its dorsal wall is bent inwards as a median fold. The
space between the limbs of this fold is the cavity of the heart (Fig.
456, E), and this space communicates with the general body -cavity,
which is a blood-space, or haeniocoele, formed by the separation of
ectoderm and endoderm, and which is a development of the slit-like
blastocoele iu the embryo. After metamorphosis the pericardial
vesicle enlarges and becomes thin-walled, and from its inner wralls,
which constitute the wall of the heart, muscular fibrils are developed,
and then the peristaltic action of the heart begins.

From the pharyngeal wall, in front of and to the sides of the
spot from which the pericardium originated, two hollow outgrowths
arise and grow backwards. These are the epicardial tubes or
epicardia. They were first described in Ciona by Newstead (1894),
whose observations were extended and corrected by Damas (1899).
According to Damas the left epicardium is larger than the right.
Both grow rapidly and form thin-walled vesicles (Fig. 456, F), which
constitute the perivisceral cavity of the adult Ciona, the primary
body-cavity being reduced to a series of blood-sinuses. The con-
joined inner walls of the epicardia form a kind of visceral peritoneum,
enwrapping heart, pericardium, and intestine. From the left epi-
cardium a plate of cells extends into the process of the body, from
which cells are budded into the test. By this plate the cavity of
this process is divided into two channels which serve as afferent and
efferent blood-streams. The epicardia in compound Ascidians are
closely connected with the process of budding ; their meaning will
be considered later.

When we last considered the pharynx it was provided with two
gill-slits on each side, which communicated with the exterior by a
lateral ectodermal invagination, the atrial opening. We also described
how these two lateral atria become merged in a common median
atrial cavity. According to Willey, these primary slits, or proto-

XVII

PROTOCHOEDATA

627

stigmata, increase in a remarkable manner at the time of meta-
morphosis (Fig. 453, C). On each side, each of the slits, at its ventral
end, curves inwards towards its fellow of the same side, so that each
takes on the form of a U. Then by a downgrowth from the dorsal

per

per

FIG. 456. — Transverse sections through the hinder part of the pharynx of a series of
larvae and just-fixed young of the simple Ascidian dona infcsti/iuHx, in order to
illustrate the development of the heart pericardium and epicardium. (Alter Kuhu.)

A, through free-swimming tadpole— the pericardium arises as a thickening of the vent nil pharyugeal
wall. B, through tree-swimming tadpole— a later stage ; the pericardium forms a sac opening into the
pharynx. C, a still later stage (still free-swimming)— the pericardial vesicles cut otf from the pharynx.
I), through a.just-lixed tadpole— the heart arises as a fold of the dorsal wall of the pericardium. E,
through an older specimen than that shown in I)— the heart has become hollow and contains lilooil
cells. F, through a still older specimen— the epical-dial tubes arise as independent ex-aginations of tin-
pharynx above the pericardium, ep.l, left epicardial tube ; ep.r, right epicardial lulic ; //. heart ; h.f.
fold which gives rise to the heart ; pli, pharynx ; jn'r, pericardium ; .< stomach.

wall, each U becomes divided into two slits, and so two new slits are
intercalated between the first two, which for this reason we numbered
No. 1 and No. 4 when we described them above. This process
reminds us of the division of the primary slits in A /////// m/: //.s by the

628 INVEETEBEATA CHAP.

growth of the tongue-bars. Then another pair of slits arise on each
side behind the original second one (No. 4), bringing the total
'number of protostigmata up to six. It is uncertain whether these
new slits (Nos. 5 and 6) arise as independent perforations of the
phary ngeal wall or by the bisection of a single U -shaped slit on each
side, but the latter hypothesis seems to be the more probable.

Since the long axis of the pharynx in the larva becomes its
vertical axis in the adult, it is clear that these six protostigmata
must form a vertical row; and, when they become subdivided, they give
rise to six transverse rows of stigmata. A stage with six undivided
protostigmata on each side has been found in many simple Ascidiaus.
The subdivision of the protostigmata has been described by De Selys-
Longchamps (1901), whose account has been confirmed by Fechner
(1907). According to him, bud-like outgrowths are formed on the
bars separating Nos. 1 and 2, 3 and 4, 5 and 6, respectively, i.e. the
tongue-bars. The outgrowths eventually unite and form the internal
longitudinal bars of the adult pharynx.

The subsequent multiplication of the stigmata of these six primary
transverse rows has been investigated by De Selys-Lougchamps(1901),
and by Dauias (1901) and Fechner (1907). It occurs by the transforma-
tion of all of them into U's, like the first-formed U's ; these have their
convexities towards the endostyle and their limbs pointing towards
the mid-dorsal Hue of the pharynx. Then these U's become divided
by dorsal downgrowths, and in this way the number of transverse
rows of stigmata is doubled. The number of slits in a transverse row
is increased by the cutting off of small portions of each slit from the
rest by outgrowths from the edges. The five large broad liars
containing blood-vessels, which separate the six primary slits, are
recognizable in the adult stage of those individuals which have been

O O

produced, not by budding, but by the metamorphoses of larvae.

The origin of the genital organs has not been clearly seen in
Ciona, but has been described in Molgula, another genus of simple
Ascidiaiis, by De Selys-Longchamps and Dainas (1902). In this
genus, in which a remnant of the cerebral vesicle containing the otolith
persists throughout life, one is able to see in the young fixed form,
when it has only two gill-slits, a small rounded mass of mesoderm
cells on the ventral side of the pharynx beneath the bar separating
the two gill-slits (Fig. 457). On the left side a similar mass is seen
in the concavity of the last curve of the intestine. As these lobes
grow they become divided into a superior mass, the rudiment of the
ovary, and a lower one, which is the beginning of the testis. The
ovary is hollow; the upper wall of the cavity is fiat, the lower
consists of the germ cells. Both rudiments grow in length and consist
of bands whose length is transverse to the length of the pharynx. The
rudiment of the testis becomes covered with rounded buds (Fig.
457, C), which finally constitute the ampullae where the spermatozoa
are produced ; ultimately the rest of the gland becomes hollowed out
to form the vas deferens. The oviduct is also formed from the

XVII

PROTOCHOPtDATA

629

upper, sterile portion of the rudiment of the ovary. In this genus
there is, therefore, & right and a left ovary, and a right and a left

hyp

oes

FIG. 457. — Illustrating the development of the genital organs in the simple Ascidian
iiiiijiii/lnides. (After Do Selys-Longchamps and Damas. )

A, young Ascidian seen I'M mi the side showing lirst trace of the genital organs. J!, the genital
rudiment of an ulder specimen showing incipient differentiation into ovary tcstes. C, ti-ansvei-se sect nm
through a genital rudiment, of a still older specimen showing the hollow ovary and the solid testes. I),
a considerably older genital rudiment showing the formation of ampullae liy the testes. n, aims ; at,
atrial cavity; e.ndxt, endostyle ; VM/I, I'udiment of genital organ; </.sl, r/x-l, the first two gill-slits; IIH/I.
liy]io]ihysial canal; int, intcstiim ; m, mouth; DCN, oesophagus; <>t, otolith; «r, ovary; at, stomach;

t, testes.

testis. It must he remembered that in dona there is only one ovary
and one testis.

630 INVERTEBRATA CHAP.

EXPERIMENTAL EMBRYOLOGY OF SIMPLE ASCIDIANS

We must now describe some illuminating experiments which
Conklin (1905, 1906) performed on the egg of Cynthia. The course
of the ordinary development of this form strongly suggests the view
that the different coloured cytoplasms, found in the unsegmented
egg, are definite organ -forming substances ; hut, of course, this
is not necessarily so, and attempts to correlate coloured substances
in the eggs of the sea-urchin, Stronaylocentrotus, with organ-forming
substances have resulted in failure.

Conklin found that the ordinary means of isolating the blastomeres
of segmenting eggs were not applicable to Cynthia. If eggs were
deprived of their membranes by shaking they perished ; and the
same result followed if an attempt were made to cut them into two
1 >y means of a sharp scalpel. If, however, the segmenting eggs were
"spurted," i.e. were sucked violently up in a pipette and blown out with
equal violence a considerable number of times, then, frequently, part
of the egg, i.e. one or more blastomeres were killed, but the survivors
continued their development and in some cases larvae emerged.

If one of the first two blastomeres be killed in this way the
survivor segments exactly as if its dead sister were still present. In
this way half-gastrulae are formed, which are like normal gastrulae
laid open lengthwise ; the edge of the cup is bordered by a quarter
circle of notochordal cells in front, and by a quarter circle
of mesenchyme and muscle cells behind. When these gastrulae
become larvae the missing parts are not regenerated. There are
muscle cells and mesenchyme cells only on one side of the body, and
though the ectoderm cells extend round so as to cover in what would
lie the naked side of the notochord, yet the notochord itself is only
formed from one row of cells, not two as in the normal larva (Fig.
458, B). At the posterior extremity of the tail the muscles of the
injured side do, to a limited extent, grow on to the uninjured side.

If the egg is " spurted " in the 4-cell stage, any one of the four
blastomeres may be killed, or the two anterior or the two posterior ;
or only one blastomere may remain alive, and this latter may be any
of the four. In what we may call anterior half-larvae, neural plate
and notochordal cells are formed, but there is no trace of muscle cells
or of mesenchyme; the neural plate is never enrolled so as to form a
nerve tube, the notochordal cells form only a plate, and invagination
does not take place. Jn posterior half- larvae, muscle and mesenchyme
cells are well formed, but there is no trace of neural plate or noto-
chord, and the endoderm forms a solid mass ; and, since there is no
notochord, the muscle cells meet in the mid-dorsal line. The mesen-
chyme cells form two masses beneath the muscle cells, and are
separated by two rows of endoderm cells. The embryo remains
rounded and shows no trace of the tadpole form. Quarter embryos
are still more imperfect, but what develops out of them corresponds

PKOTOCHOKDATA

631

exactly to what would have developed out of them had their sister
blastomeres remained alive.

Conklin, therefore, may fairly claim to have proved that these
coloured cytoplasms are definite organ-forming substances. He has
proved that similar substances exist in the eggs of Ciona, Molgula,
and Phallusia (1911), only that these substances are not distinguish-
able from one another in the living egg, but require staining to
differentiate them from one another.

But now the question arises: if the organs of the larva are
determined by substances situated in definite regions of the unseg-
mented egg, whence do those substances come ? The answer to this

ph

p.mch

FIG. 458. — Illustrating the resiilt of the development of single blastomeres of the 2-cell
stage of the egg of Cynthia, partita. (After Conklin.)

A. frontal longitudinal section of young tadpole of Cj/miTiia partita developed from normal egg. B,
frontal longitudinal section of young tadpole of Cynthia. i<n,iitn developed from 2-cell stage in which
the' left blastomere was killed, u.mt-h, anterior nieseneliyine (corresponding to the supej im niesenehyme
of Fig. 440); r/i, notochord ; ect, ectoderm ; -HIS, mesodermal band; jili, pharynx; p.in<:h, posterior
niesenchyine (corresponding to the. inferior mesenchyme of Fig. 446).

is, that one of them, the clear ectoderm-forming substance, is
actually contained in the nucleus. Further, Schaxel (1910) has shown
that, in the developing oocyte, chromatin is emitted from the nucleus,
and that the slaty-blue yolk spherules grow at the expense of these
chromatin particles. Hence we may boldly assert that the cytoplasm
of the ripe egg is differentiated by the egg-nucleus.

But although the substances are formed under the influence of the
egg-nucleus, they are arranged under the influence of the sper-
matozoon. As we have seen, the entering spermatozoon drags the
yellow substance after it, and thence determines the position of the
muscle-forniing material. If two spermato/oa enter the egg, then tin-
yellow substance forms two aggregations instead of one. In the egg

632 INVEETEBRATA CHAI-.

of Cynthia, partita Nature lias provided us with an ocular demon-
stration of the existence of organ-forming substances.

OTHER GROUPS OF ASCIDIANS

We must now take a brief glance at the modifications which the
life-history which we have described undergoes in other groups of
Ascidians. As already indicated, the other simple Ascidians, so far
as they have been examined, have a development which is, cell
for cell, identical with that of Cynthia. To this statement,
however, certain species (but not all) of the genus Molgula form an
exception.

In Molgula, ampulloides, as described by Damas (1902), the early
development is identical with that of Cynthia, but the tail rudiment
remains short, and the hinder part of the nerve tube, the notochord,
and the tail muscles, undergo degeneration before the larva escapes
from its membrane. The notochord and muscles are indeed converted
into a mass of fatty cells 'which forms a rounded protuberance at one
side of the larva. The larva cannot swim, and tumbles at once to
the bottom, where it attaches itself by long finger-like processes of
the test. The atrial cavity is formed by a single mid-dorsal involution
of the ectoderm, which forks below into right and left pouches ; each
of these pouches comes into contact with two evaginations of the
pharyngeal wall which are the endodermal portions of the first two
gill-slits on either side.

In the Ascidiae compositae, the larva differs from that of simple
Ascidians in the precocious appearance of adult features ; thus the
atrial cavity generally attains the form of a single dorsal cavity with
median opening, whilst the larva is still free-swimming. The chin
region of the larva is already disproportionately large, and the mouth
and atrial openings are consequently close together. In some cases,
as for instance in Clavelina, the eggs are small ; but in other cases,
such as Distaplia, the eggs are larger and more yolky, and the
endoderm is in the form of a solid mass of cells like those at the
lower pole of the frog's egg. In such cases the archenteric cavity is
formed by a separation of these cells from one another, not by an
invagination, and there is never an open blastopore. The neuropore
never closes, but persists until it becomes converted into the opening
of the sub-neural gland.

In Ascidiae luciae, represented by the single genus Pyrosoma,
the eggs are still larger and each individual produces only one egg.
The yolk is so massive that it remains largely unsegmented, and its
development is, like that of Cephalopoda, of the meroblastic type, in
which a germ disc or blastoderm rests on an unsegmented mass of
yolk. The test cells, or follicle cells, wander inwards amongst the
blastomeres during the progress of segmentation (Fig. 459). Many
of them die and degenerate and are used as food, but according to
Julin (1912), who has given the latest and most satisfactory account

XVII

PEOTOCHOEDATA

633

of the development of this form, many of the test cells survive and
give rise to the phosphorescent organs of the adult (ji/ws, Fig. 466).
In the yolk there are nuclei which are. derived by division from

tc

him

FIG. 459. — Suction through the segmenting of I'lirosiima r/ii/dnicum at the stage of
thirty-six lilastomeres. (After Juliii.)

lit HI, blastoincre ; ./; follicle cells ; t.<; test cells— some have wandered in unionist, (lie
lilastonieres ; ;/, unsegmented yolk.

the nuclei of the blastomeres, and which we may term yolk cells.
They are surrounded by islands of cytoplasm (y.c, Fig. 460).

Between the blastoderm and the yolk a cavity appears which is
the archenteric cavity, and at this stage, according to Julin, the
blastoderm consists, throughout the greater part of its extent, of

Ic

FIG. 460. — Longitudinal sections through two embryos of Pyrosom« '////"///</'///, in order

to show the formation of organs in the Cyathozooid. (Alter Julin.)

A, seetion tlinmgli younger embryo. 13, section tlmmxli older embryo. I'm/, endodei-ni t'oi'niiii.u m.,1
of archenteron and beginning to extend on to its floor ; /, follicle \\itli nuclei ; »./>. nei ve plate formed
by an ectodermic thickening which becomes invaginatc.l ; per, pericardia! tniie; /.//. |ihaiyn\; t.<; test
cells ; H.C, yolk i ells.

two layers. The outer of these, layers constitutes the ectoderm,
and the inner, which forms the immedinte roof of the archenteric
cavity, is endoderni. The two layers pass into each other along a
definite lip which Julin identities with the dorsal and anterior lip of the
blastopore, corresponding to the region x in the gastrula of Amphioxus.

634

INVEKTEBEATA

CHAP.

In later stages of development the archenteric cavity acquires a
floor of cells, produced mainly by the increase in number and adhesion

of the yolk cells, which repre-
sent the white cells at the
lower pole of the i frog's egg.
Meantime the ectoderm,
extending out from the
anterior edge, i.e. the opposite
side of the blastoderm to that
of the region x, grows as a
simple sheet of cells over the
yolk, and so eventually the
blastopore is closed. The arch-
enteron becomes the pharynx,
no tail endoderm being formed.
The formation of organs
is now begun. The nervous
system arises as a median

&'

arises

dorsal invagination of ecto-
derm in front of the region x.
Behind it a median pit arises,
which is the rudiment of the
cloaca or median atrial open-
ing. On the sides of the
pharynx two ectodernial
grooves are formed which are
the atrial imaginations.
They become largely separated
from the exterior so as to form
tubes with narrow openings
directed dorsally. As growth
per Soes on their openings are
forced farther and farther
upwards, and become involved
in the median invagination,
alluded to above, which forms
the cloaca. Each atrial tube

FIG. 461.— Two embryos of Pi/rosomagi!/<(ii/<'iim, communicates With the
viewed from the dorsal surface in order . . • -,

to show the formation of organs in the pharynx, On its lUlier Side,

Cyathozooid. (After Julin. )

A, younger embryo. B, older embryo \vliii-li lias
already formed a stolon, at, common atrium formed by
bhe junction of the two atrial tubes; nt.I, left atrial
tube; nt.n, obliterated portion of the left atrial tube;

n

by a narrow slit which is a

rudimentary gill-Slit.

Tl-.,-> nn-winavrliiim >ii-iut'« fl«
riCardlUm .1. Lbtb a,

tWO Ventral OlltrOVVtllS OI tlie

nt.r, right atrial tube; en<7*/, endostyle ; H, heart ; n.p, pharynx which,

'

nerve-plate; per, pericardial sac ;StoJ, stolon.

speedily fuse into One and

constitute a single vesicle. The single vesicle sends out two pro-
longations, a right and a left ; of these the left becomes solid and
atrophies, but the right swells and forms the persisting heart

xvii PROTOCHORDATA 635

and pericardium of the embryo, whilst the rest of the vesicle
disappears.

On the floor of the pharynx the endostyle is formed as a large
median groove with thick prominent lips, and behind this there
grows out what Julin calls a prolongation of the pharynx, but which
we (following Hjort) regard as two enormous epicardial tubes fused
together. This prolongation curls itself round the yolk, and from it,
in a manner to be described shortly, the first buds arise. It remains
to be added that, when the atrial involutions have become united with
the median cloacal opening, the two rudimentary gill-slits disappear
and are replaced by a single dorsal median opening into the pharynx.

If this description has been followed, it will be seen that the first
individual to be formed by the development of the fertilized egg in
Pyrosoma is of a very degenerate character. It possesses no trace of
a mouth or of an intestine, and no trace of notochord or caudal
muscles. In the neighbourhood of the blastoporal rim a ring of
mesenchyme is produced. This vestigial individual is called the
Cyathozooid, in order to distinguish it from the more perfect
individuals produced by budding.

When we pass to the Thaliaceae we find, in the genus Salpa, a
form in which the egg develops directly into the adult form without the
intervention of a tailed larval stage. In this case the egg remains
in the oviduct in the mother, only moving down from the ovary to
a brood-chamber at the mouth of the oviduct ; whereas in Pyrosoma
the egg is spawned into the sea. The egg, after dividing into a few
blastomeres, is invaded by follicle cells which wander in between the
blastomeres and surround them. According to Salensky (1883), the
blastomeres perish and the embryo is built up out of follicle cells.

In view of the fact that Salensky (1891) has made somewhat
similar statements about Pyrosoma, in which he alleges that test cells
become blastomeres, and that Julin has shown this view to be
erroneous, it may be doubted whether Salensky 's statements about
Salpa are any more reliable. Moreover, in the case of Salpa, it is very
difficult to distinguish between blastomeres and follicle cells. It
seems more probable that it is the follicle cells which perish and are
eaten by the separated blastomeres, which then reunite. Similar
cases of the separation and subsequent reunion of blastomeres are
known amongst Platyhelminthes.

The solid mass of cells constituting the embryo sits, rider-like, on
a knob of maternal tissue, inside which there is a great development
of blood-vessels. This knob constitutes a nutritive organ or placenta.
The blood of the mother seems to diffuse through to the tissues of
the embryo. An ectoderm is differentiated from the peripheral
layer of the embryonic mass, and the placental knob is overgrown by
a flap of this layer. From a thickening of the ectoderm the nervous
system is developed.

Two lateral portions of the inner or endodermic mass become
distinguishable from the rest, by their histological character, as

636

INVERTEBRATA

CHAP.

mesoderm. A posterior mass is the rudiment of the elaeoblast, a
protuberant mass of fatty globules which probably represents the last
vestige of the lost larval tail. The pharyngeal cavity then appears
in the centre of the median portion of the endodermic mass. It is
nearly divided into two by a median dorsal infolding, the rudiment
of the adult "gill." The cloacal cavity appears as a median invagina-
tion of ectoderm, and unites with the pharynx at the sides of this
so-called " gill."

The nervous system separates from the ectoderm and becomes
hollowed out, showing a transient indication of division into three

mas c cure

m

FIG. 462. — The embryo of Salpn fusiformis attached to the maternal placenta, seen from

the side. (After Salensky.)

a, anus ; at, atrial opening ; d.l, dorsal lamina (remnant of dorsal wall of pharynx) ; el, elaeoblast ;
endst, endostyle ; H, heart; h.j>, blood-forming organ in the placenta; //.i/yi, hypophysial canal; hit,
intestine ; m, mouth ; »n/si.-.oi/r, circular bands of muscle ; n.p, nerve ganglion ; UP.S, oesophagus ; per,
pericardium ; pi, placenta.

chambers, which have been compared to the three brain-vesicles of
the embryos of higher Vertebrates (n.t, Fig. 464). The, neural tube
becomes connected with the pharynx close to where the mouth is
formed as an invagination. The mesodermic mass on each side gives
rise to the characteristic hoop-like muscles which are the adult organs
of locomotion. The elaeoblast is now gradually absorbed, the embryo
wrenches itself loose, breaking off the placental knob and carrying
away with it this portion of the maternal tissues embedded in its
body, where it is gradually absorbed, though its remains can be
recognized for a long time.

In Dolioluni, the other well-known genus of Thaliaceae, the egg
is shed into the sea, and its early development seems to resemble that

xvn PEOTOCHOKDATA 637

of simple Ascidians ; hut the tailed larva shows some quite peculiar
features. • The pharynx remains quite small, and there is an enormous
ectodermic vesicle at the root of the tail which ohviously serves for
tlotatiou. In front of this there is a mesodermic mass, and 1 lehind it
are situated two mesodermic masses, and behind these again the
notochord with its longitudinal muscles.

The nervous system is represented by a very large solid mass of
cells — a brain-vesicle being apparently absent. The front mesodermic
masses give rise to the hoop-like muscles of the pharynx ; the atrial
cavity arises as a median invagina.ti.on, forking below, and each fork
communicates with the pharynx by a series of undivided "proto-
stigmata." As the hoop-like muscles develop the great ectodermic
vesicle shrinks, and finally the embryo differs from the adult only in
carrying tail and notochord. These are finally absorbed and the
development is then complete.

The Ascidiae luciae and the Thaliaceae agree in being purely
pelagic forms which pass the whole of their lives swimming in the
open sea. The tailed larva cannot, therefore, fix itself to any solid
substratum. To meet these altered conditions the development
undergoes three different modifications in Pyrosoma, Salpa, and
Doliolum respectively.

In Pyrosoma the embryo is a mere sketch of the typical larval
form ; it begins to bud before it is half-developed, and founds the
colony round the remains of the yolky egg, after which the original
person disappears. In Salpa the egg must have originally developed
into a tailed larva, but this larva fixed itself to the maternal atrial
wall at the mouth of the oviduct, and there grew till it was ready to
break loose. Finally, in Doliolum, the larval organs, tail, and noto-
chord are retained till the adult form has been reached.

ASEXUAL REPRODUCTION IN UROCHORDA

The asexual reproduction of the Urochorda is a most fascinating
subject, and has attracted an immense amount of research which is
embodied in an extensive literature. The whole subject, however,
has been reviewed in a most masterly way by Hjort (1896), whose views
have stood unchallenged for the last eighteen years. Bitter (1897),
the only worker who has since then published an important paper on
the subject, confirms Hjort in all important matters and endorses his
views. It would be waste of time, therefore, to trouble the. reader
with the views of earlier workers whose ideas on the subject were by
no means clear. Pizon, however, both before (1891) and since Hjort's
paper appeared (1905), has made a special study of the extraordinary
condition of affairs prevailing in the family of compound Ascidiaus
termed Diplosoniidae.

According to Hjort, then, there are two main types of bud-
formation found amongst Urochorda, which, so far as we. can see,
must have been independently evolved. These arc; pallial budding,

638

INVERTEBKATA

CHAP.

e.1

sang

found in Botryllus and its allies ; and stolonial budding, found
amongst all other Tunicata.

Stolonial budding has been thoroughly studied in the genus
Clavelina by Van Beneden and Julin (1887), and the results of
these authors have been completely confirmed by Hjort's studies on
Perophora and Distaplia. In all three genera the two epicardial
cavities grow out from the pharynx, even in the free-swimming

larva, and as soon as fixation takes place
they become long and fuse at their distal
ends into a single cavity. Van Beneden
and Julin imagined that the pericardium
was cut off from this cavity, but that, as
we have seen, is a mistake: the pericardium
originates earlier, as a median evagination
of the pharynx. The conjoined epicardial
cavities collapse, and their walls then
form a thin plate of cells, which projects
into a ventral protrusion of the ectoderm
which forms the stolon. It forms a
median septum in this stolon, which
divides the afferent and efferent blood-
streams from each other; but as this
septum does not reach quite to the tip,
the streams pass into each other here.

New buds are formed as lateral
branches of the stolon. Branches of the
epicardial septum are continued into these
branches, and these pieces of the septum
develop into sacs by the reappearance
of the lost cavity of the epicardial tube
(Fig. 4Go). The young bud is therefore
FIG. 463.— Budding stolon of formed from a double - walled vesicle,
Perophora listen showing the Of whjch the outer layer is furnished by

development of buds from
the septum of the stolon.
(After Hjort.)

ectoderm, whilst the inner
layer arises from the epicardial tube.

?-, wood ; c./, external layer of bud Between these two layers are contained
rudiment ; i.z, internal layer of bud a certain number of loosely aggregated

ii.diMHMit; win,/, blood-space; «<?>, ,||(JS()(](,rm oells
septum of the stolon, a double layer

Mtv,-iis. As Hjort shows, the building up of

the organs of the young "blastozooid,"

as the "person" produced by budding is termed, takes place in
a very different manner from that in which it occurs in the
embryo produced from the fertilized egg. Thus the atrial cavity
arises by the downgrowth of two septa, which divide the inner
vesicle into a median and two lateral portions ; the median is the
rudiment of the. pharynx, the lateral of the atrial cavities. The
nervous system arises as a dorsal hollow outgrowth of the inner vesicle,
at the border of the left and median divisions ; it grows forwards and

XVII

PROTOCHOKDATA

G39

acquires a new opening into the vesicle at the front end. This
new opening becomes the sub-neural gland, or hypophysial tube;
the other opening disappears. No protostigmata are formed ; the
definitive stigmata arise as small perforations of the pharyngeal wall.
The intestine arises as an outgrowth from the hinder wall of the

FIG. 464. — Stages iu the development of the bud of Distapli/t iniifjnilnri-i/. (After lljcnt.)

A, lateral view of young bud in which the two atrial rudiments are still separated. B, dorsal view
of young bud in which the two atrial rudiments are still separated. C, dorsal view of older hud in which
the atrial rudiments have united in the mid-dorsal line. nt.l, left atrial rudiment ; nt.r, right aliial
rudiment ; ep, epieai'dial tubes ; int, rudiment of intestine ; «.', nerve tube — rudiment i it1 adnlt ganglion ;
LI r, ovary ; pli , pharynx.

pharynx ; the pericardium as a median evagination of the ventral
wall of the same organ. The muscles and the genital organs arise
from the mesodermal cells (Fig. 464).

In Pyrosoma, Salpa, and Doliolum, the stolon arises in just
the same manner as in Clavelina. In Pyrosoma, as we have already

640 INVEKTEBKATA CHAP.

learnt, the rudimentary embryo is called the Cyathozooid ; the stolon
gives rise to four " blastozooids " known as "Ascidiozooids," which
form a cycle according to Julin (1912). The ectodermal pe'ribranchial
or atrial tubes of the Cyathozooid extend backwards into the
Ascidiozooids, and give rise to the atrial cavities of these persons by
segmenting off four pieces; but this, according to Hjort, does not hold
for buds subsequently produced. The atrial cavities of the later buds
arise from solid proliferations of the walls of the inner vesicle, which
subsequently become hollowed out, and obviously correspond to the
lateral compartments of the inner vesicle of the bud of Distaplia.
The nervous system arises as a pair of outgrowths from these two
lateral vesicles, which grow inward and unite in a mid-dorsal tube,
which then forms a new connection with the central vesicle in front.

gang, ad

~U^>^.

\, endsl

^^^^T "

at-

FIG. 465. — Lateral view of old luul of Distaplia maynilarva. (Alter Hjort.)

at, opening cil' single atrial cavity; endst, endostyle ; ;/K «</•<"', adult ganglion, a thickening of the
dorsal wall of tin- hypnphysial tube ; g.s, Mist gill-slits appearing as perforations of the pharyngeal wall ;
hyp, hypophysial tube ; m, mouth.

The posterior connections become solid and form a transverse
nerve (Fig. 466).

In Salpa, the buds formed by the stolon remain connected with
one another for a considerable time, and constitute in this way a
train of " blastozooids," which is dragged along by the oozooid, as
the person produced from the egg is termed, and which thus acts as
engine to the train. As the blastozooids attain a respectable size
they drop off and lead independent lives; they constitute the sexual
generation.

In Doliolum the buds break loose from the stolon whilst they are
in a most immature condition, and climb by amoeboid movements
over the surface of the parent, till they reach a posterior horn of the
test situated in the mid-dorsal line. To this horn they attach them-
selves in three longitudinal lines. Those in the lateral lines become
trophozooids, without muscles and with wide mouths, which serve
to nourish the colony ; those in the median line become like the

XVII

PKOTOCHOKDATA

641

parent, except that they have a different number of muscular bands.
It is uncertain whether these median buds, termed phorozooids,
break loose and develop into individuals with sexual organs, or
whether they produce ventral stolons from which the true sexual

generation arise as buds.

phos

at-

FIG. 466. — Primordial colony of Pyrosoma giganteum consisting of four Ascidiozooids
coiled round the degeneration Cyathozooid. (After Julin.)

Asfl-Ase1, the four Ascidiozooids; at, common atrial openings of an Asddiozooid and also of the-
Cyathozooid ; at.t, persistent atrial tube ; t';/, Cyathozooid ; H, heart of Cyathozooid ; m, mouth of
Ascidiozooid ; np, nerve-plate of Ascidiozooid ; per, pericardial sac of Ascidiuzooid ; jiW-, phosphori-scent
organ consisting of an agglomeration of test-cells ; y, unsegmented yolk of Cyathozooids.

The buds of Doliolum are in so far peculiar that the inner vesicle
is represented by a solid mass of cells, in which strings of cells are
gradually differentiated which develop into pharynx, atrial cavities,
muscular tissues, and nervous system.

In Botryllus and its allies the buds arise as two layered vesicles,
and their development is exactly what has been described in the case
of Distaplia. But whilst the outer wall of the vesicle arises as an

VOL. i 2 T

642

INVEETEBKATA

CHAP

evagiuation of the parent ectoderm, the inner arises as an evagination
of the parent atrial cavity (Fig. 467). No epicardia exist in the
Botryllidae. The young " oozooid " produced from the egg perishes
after having given rise to the first buds, which then give rise to the
rest of the colony (Fig. 467).

Finally, in the family Diplosomidae we have a most extraordinary
condition of affairs, which has been elucidated by the researches of Pizou
(1905). Budding begins by the development of epicardia in the embryo,
before the larva escapes from the egg-membrane. During the larval

ale ff~s

ird

FIG. 467. — Bud of a Botryllid almost completely developed and bearing two young buds ;
seen from the dorsal side. (After Hjort. )

at.c, atrial cavity ; ft, young bud rudiment ; e.l, external layer of young bud rudiment ; i/.s, gill-slits ;
H, heart ; i.l, internal layer of young bud rudiment — this is seen to be a prolongation of the lining of the
atrial cavity of the mother ; int, intestine ; m, mouth ; n.t, nerve tube (including hypophysial tube) ; or,
ovary ; per, pericardium.

life a perfect blastozooid is produced, so that the tailed larva possesses
two branchial sacs, two intestines, and two nervous systems, but only
one notochord. One of the nervous systems, i.e. of the blastozooid, is
devoid of a sense-vesicle. When the larva fixes itself budding
continues in both blastozooid and oozooid. The epicardial stolon,
however, produces only a pharynx, nervous system, and the rudiment
of an oesophagus. This oesophagus, instead of developing a new gut,
joins the oesophagus of the parent. At the same time an independent
bud is produced as an evagination of the rectum (Fig. 468, B), and
forms a new rectum though still retaining its connection with the
old one.

Then one of two things may happen. Either a new stomach and

XVII

PEOTOCHOEDATA

643

intestine are developed from a third Imd, which arises from the old
oesophagus just where the epicardial Imd joins it (Fig. 468, D) ; and

oes'

oes

oes1

oes*

int* ep

FIG. 468. — Four stages in the budding of, a Diplosoiuid Ascidian. (After Pizon.)

A, the oozooid (i.e. the organism produced by the metamorphosis of the larva) has produced by
separate buds a new pharynx and oesophagus and a new intestine. 15, the new organs ihave greatly
increased in size. C, the pharynx of the oozooid is reduced to a degenerate mass, its oesophagus and
intestine have disappeared, but the second pharynx has produced by budding a I bird pharynx ; a second
stomachic loop has been produced. D, the third pharynx has increased in si/e and has developed an
oesophagus and a third intestine has been produced. A second heart has been produced from the second
pharynx, and the second stomachic loop has become functional. < »./.< endostyle; ,</i, epicardial out-
growths from second pharynx ; H\, //•_>, the hearts ; inn, hit-, hit", the intestinal rudiments; 01*1, oes",
ops3, the oesophageal rudiments ; j>/i', />//-, ;>/V;, the three pharynxes ; at] , at-, t he t wo stomachs.

so a compound organism arises with two branchial sacs joining in a
common gut, which then bifurcates into two intestinal buds, which
reunite at their distal ends, only to bifurcate again into two recta.

644 INVEETEBEATA CHAP.

Or, the old pharynx, oesophagus, and rectum degenerate, leaving the
new pharynx and rectum in connection with the old intestinal coil.
In the first case the compound organism separates into two persons
by the splitting of the common pieces of oesophagus and intestine,
and this splitting takes place in such a way that the old intestine
and rectum remain connected with the new pharynx, whilst the old
pharynx enters into connection with the new intestinal coil. In the
second case the person is "rejuvenated " by the substitution of a new
pharynx and rectum for the old structures.

It will be thus seen that the budding of Urochorda calls up the
same kind of problem as does the budding of Polyzoa, but in an even
more acute form. In the Polyzoon bud two totally distinct organs,
the circle of lophophoral tentacles, which are protrusions of the
ectoderm, and the gut which in the larva is formed from endoderm,
arise from the same ectodermal rudiment in the bud and are known
collectively as the "polypide." This polypide degenerates from time
to time, and is replaced by a new one developed in the same way as
the old. In the larva of Urochorda the atrial cavity and the nervous
system arise from the outer layer, but in the bud they originate from
the inner layer. In stolonial budding the inner layer of the bud
arises from the parental endoderm, but in pallial budding it arises
from the parental ectoderm. Finally, as we have just seen, in
Diplosomidae three distinct bud rudiments coalesce to form a new
individual, and the part of the individual produced by one of these
buds can degenerate and be replaced like the " polypide " of Polyzoa.

How are these facts to be reconciled with the doctrine of germ
layers ? If the distinction between ectoderm and endoderm be the
first and fundamental differentiation of egg sub stances, how can an
ectodermal organ, like the nervous system in Urochorda, be produced
from endoderm ; or, vice versa, how can an endodermal organ, like the
gut in Polyzoa, be produced from ectoderm.

Hjort's suggested explanation of this anomaly is ex tremely plausible.
He first of all gets over the difficulty that the inner layer of the bud
is formed from endoderm in Clavelina, Distapha, Perophora, but from
ectoderm in BotryUus. The double-walled vesicle, he maintains, is to
be regarded as the starting-point of the bud as a new organism, and
is equivalent to the ovum, which is the same whether it appears in
ectoderm or eudoderm. But the outer wall of the bud is in all cases
formed from the outer ectoderm of the parent, which is a highly
specialized tissue committed irrevocably to producing cellulose, and
which is therefore incapable of being modified into nervous tissue.
The ectoderm of the embryo, on the contrary, consists of compara-
tively undifferentiated cells, capable of plastic modification in many
directions. The inner layer of the bud, whether derived from
epicardium or atrial membrane, consists of cells in a plastic condition,
and therefore gives rise to all the organs of the " blastozooid " except
the cellulose-producing ectoderm. In the bud of the Polyzoon, if we
follow an analogous course of reasoning, the ectodermal outer layer

xvii PROTOCHOEDATA 645

consists of cells in a plastic condition, and all the organs of the bud
must arise from it, since endoderm in the bud is conspicuous by its
absence, i.e. there is no inner layer.

Another way of looking at the matter, however, occurs to one on
thinking over the lessons learnt from the development of the egg of
Cynthia. We have learnt that the cytoplasm of the egg in this
form contains specific organ - forming substances ; and that the
germinal layers and the rudiments of the organs in the developing
embryo are distinguished from one another by the possession of
different organ-forming substances. We can see this in Cynthia ; the
presumption is that such substances distinguish the germinal layers
from one another in the case of embryos right throughout the animal
kingdom, though the chemical differences between them do not usually
reveal themselves to our eyes by different colours. The formation of
these substances we have seen to be the work of the nucleus of the
developing oocyte, while their final arrangement is due to the sperma-
tozoon, or rather, we might say, to the zygote-nucle.us, for the sperma-
tozoon and egg-nucleus come together by a mutual attraction. But,
once the definite location of these substances is fixed, it appears as if
the nuclei of the segmenting egg were powerless to affect them.
Pressure experiments on the eggs of Echinoderms, and even on highly
specialized eggs like that of Aems, show that these nuclei can be juggled
about like a handful of marbles, and made to change places with each
other without affecting the disposition of the organs of the embryo.
Thus the specific quality of organs depends on the cytoplasm of the
egg, and not on its nuclei.

But it seems certain that this passive condition of the nuclei is
only a transitory phase. Leaving aside the obvious fact, that when
the generative cells are formed the nucleus must resume its active
role, there is evidence to show that the specific ferments which
characterize certain gland cells, such as the pancreatic cells, are
formed out of particles emitted by the nucleus. It is then reason-
able to assume that, in the formation of buds, the nuclei again become
active and manufacture organ-forming substances in the cytoplasm,
but it does not follow that the arrangement of these will be the same
as in the egg. It may be that the possibility of the formation of
these substances is bound up with a certain quality of the cytoplasm,
and the nuclei in the outer layer of the bud may attempt to do this
and may fail. We may reflect that in dona, if any of the cells of
the developing embryo be killed, a portion of the tissues of the larva
will be missing, and that the larva is unal >le to make good the defect ;
and that yet, if the larva be allowed to metamorphose into an Ascidia n,
and the whole upper part of the young dona, including the ganglion,
be bitten off, the stump can regenerate the missing parts. That-
being so we can realize the difference between an active and an
inactive condition of the nuclei.

It lias been hinted above that, since CHon« possesses two large
thin-walled epicardia, the view has been held that it and the other

646 INVERTEBKATA CHAP.

simple Ascidians once had the power of budding and lost it. The
study of the larvae of simple Ascidians does not bear out this view.
In the general disposition of their organs, and in the formation of
their stigmata, they are more primitive than the simplest compound
Ascidian, Clavelina. If, then, the epicardia were not originally connected
with budding they may possibly represent anterior coelomic sacs—
perhaps the collar-cavities since they lie externally to the other viscera.
The origin of the pericardium as a single median evagination of
the pharynx is, however, hard to explain. The pericardium of the
higher Vertebrata is formed from a portion of the splanchuocoele
behind the branchial region, and this splanchnocoele is simply the
lower end of the front part of the conjoined trunk -cavities. Now the
trunk - cavities of the Urochorda are mainly represented by the
longitudinal muscles of the tail, and by the so-called anterior mesen-
chyme cells which form the mesoderm of the adult, and actually, for
some time, form part of the lateral walls of the embryonic gut. Yet
there can be little doubt that the pericardium and heart of Urochorda
are homologous with those of higher vertebrates ; they are situated
in the same position in the adult, and the heart, by its shape, reminds
one of the S-shaped heart of the higher vertebrate embryo.

Perhaps the only suggestion which can be offered is this. The
pericardium is held back in development ; it does not develop until
the later part of larval life, and its origin from the pharyngeal wall
may represent the outgrowth of the trunk-cavities from the archeuteric
wall of Amphioxus. We may suppose that the front portions of
these cavities develop late, and independently of the hinder portions,
just as we explain the larval and adult mouths of Echinodermata as
the two parts of an ancestral mouth, one of which is held back in
development. A detailed study of the development of Larvaceae
would probably throw light on this question.

In any case there can be no doubt that the ancestor represented
by the Ascidiau tadpole, and in certain degree by the adult in the
group Larvaceae, possessed a well-developed brain-vesicle with hemi-
spherical visual optic lobes, a hypophysis or pituitary body opening
into the stomodaeum, also a well-developed tail, and a definite heart ;
and that in all these respects it was far in advance of the stage repre-
sented by Amphioxus. The distance which separates the points at
which Amphioxus and Urochorda diverged from the main stem of
Vertebrata, is almost comparable to that which separates the points
of origin of Amphioxus and Enteropneusta from the same stem.

[Note. — It is necessary that this group of animals, lying, as it does,
on the borderland of both Invertebrata and Vertebrata, should be
treated by the uuthors of both Vol. I. and Vol. II. ; and, as each author
is solely responsible for the facts and opinions contained in his book,
the reader must be prepared to find that the views adopted by each
author, especially regarding this overlapping group, may not wholly
coincide. — EDITOE.]

xvn PKOTOCHOKDATA 64*7

LITERATURE REFERRED TO

HEMICHORDA

Bateson, W. The Early Stages in the Development of Balanoglossus. Quart.
Journ. Mie. SeL, vol. 24, 1884.

Bateson, W. The Later Stages in the Development of Balanoglossus (Dolichoglossus]
kowalevskii, with a suggestion as to the Affinities of the Enteropneusta. Quart. Journ.
Mic. Sc., vol. 25, 1885."

Davis, B. M. The Early Life History of Dolichoglossus pusillus. Univ. of California,
Publ. Zoo]., vol. 4, No. 3, 1908.

Herder, K. Zur Entwicklung von Balanoglossus clavigcrus. Zool. Anz., vol. 34,
1909.

Metschnikoff. Ueber die Metamor])hosen einiger Seethiere. Zeitschr. f. wiss. Zool.,
vol. 20, 1870.

Morgan, T. The Growth and Metamorphosis of Tornaria. Journ. Morph.,
vol. f», 1891.

Morgan, T. The Development of Balanoylossus. Ibid., vol. 9, 1894.

Ritter, W. On a new Balanoglossus Larva from the Coast of California, and its
possession of an Endostyle. Zool. Anz., vol. 17, 1894.

Spengel. Die Enteropneusten des Golfes von Neapel und der angrenzenden
Meeresabsehnitte. Fauna and Flora. — Golf Neapel, No. 18, 1894. ,

CEPHALOCHORDA

Balfour. Text-book of Comparative Embryology, vol. i. 1881.

Boveri. fiber die Bildungsstatte der Geschlechtdriisen und die Entstehung der
Genitalkammern beim Amphioxus. Anat. Anz., 7th February 1892.

Cerfoutaine. Reeherches sur le developpement de V Amphioxus. Arch, biol.,
vol. 22, 1907.

Goldschmidt. Amphioxus. Wiss. Ergeb. Deut. Tiefsee Expedit. "Valdivia,"
vol. 12, 1905.

Goodrich. On the Structure of the Excretory Organs of Amphioxus, Pts. 2-4.
Quart. Journ. Mic. Soc., vol. 54, 1909.

Hatschek. Studien iiber die Entwicklung des Amphioxus. Arb. Zool. Inst. "VVien,
vol. 4, 1881.

Hatschek. fiber den Schichtenbau von Amphioxus. Anat. Anz., 3te Jahrgang,
1888.

Kowalevsky. Entwicklungsgeschichte des Amphioxus lanceolatus. Mem. Acad.
St-Petersbourg, series 7, vol. 11, 1867.

Kowalevsky. Weitere Studien iiber die Entwicklungsgeschichte des Amphioxus
lanceolatus. Arch. mik. Anat. vol. 13, 1877.

Lankester and Willey. .The Development of the Atrial Chamber of Amphioxus.
Quart. Journ. Mic. Soc., vol. 31, 1890.

Legros. Sur quelques cas d'asyntaxie blastoporale chez 1' 'Amphioxus. Mitt. Zool.
St. Neapel, vol. 18, 1907.

Lwoff. Die Bildung der primaren Keimbljitter und die Entstehung der Chorda
und des Mesoderms bei den Wirbeltieren. Bull. Soc. Nat. Moscou, 1894.

MacBride, E. W. The Early Development of Amphioxus. Quart. Journ. Mic.
Sc., vol. 40, 1898.

MacBride, E. W. The Formation of the Layers in Amphioxus, and its Bearing on
the Interpretation of the Early Ontogenetic Processes in other Vertebrates. Ibid., vol. 54,
1909.

Morgan and Hazen. The Gastrulation of Amphioxus. Journ. Morph., vol. 16,
1900.

Van Wijhe. Beitrage zur Kopf region des Amphioxus lanceolatus, 1901.

Willey. The Later Larval Development of Amphioxus. Quart. Jmirn. Mic. Sc.,
vol. 32, 1891.

UKOCHORDA

Castle. The Early Embryology of dona intcstinalis. Bull. Mus. Harvard, vol.
27, 1894.

648 INVERTEBRATA CHAP, xvn

Conklin. The Orientation and Cell-lineage of the Ascidian Egg (Cynthia partita).
Journ. Acad. Sc. Philadelphia, series 2, vol. 13, 1905.

Conklin. Mosaic Development in Ascidian Eggs. Journ. Exp. Zool., vol. '2, 1905.

Conklin. Does Half of an Ascidian Egg give rise to a whole Larva ? Arch. Entw.
Mech., vol. 21, 1906.

Conklin. The Organisation of the Egg and the Development of Single Blastomeres
in Phallusia mammillata. Journ. Exp. Zool., vol. 10, 1911.

Damas. Les Formations epicardiques chez dona intestinalis. Arch, biol.,
vol. 16, 1899. ,

Damas. Etude du sac branchial chez Ciona intestinalis. Ibid., vol. 17, 1901.

Dainas. Reeherches sur le developpement des Molgules. Ibid., vol. 18, 1902.

Fechner. Beitriige zur Kenntnis der Kiemenspaltbildung der Ascidien. Zeit. f. wiss.
Zool., vol. 86, 1907.

Hjort. Germ-layer Studies based on the Development of Ascidians. Zool. Res.
Norwegian North Atlantic Exped., Christiania, 1896.

Julin. Recherches sur le developpement embryonnaire de Pyrosoma gigantcum.
Zool. Jahrb., Sujipl. 15, vol. 2. Festschr. zum 60ten Geburtstag Spengel, 1912.

Kowalevsky. Entwicklungsgeschichte der einfachen Ascidien. Mem. Acad.
St-Petersbourg, series 7, vol. 10, 1866.

Kowalevsky. Weitere Studien liber die Entwicklung der einfachen Ascidien.
Arch. mikr. .Anat. , vol. 7, 1871.

Kuhn. Uber die Entwicklung des Herzens der Ascidien. Morph. Jahrb., vol. 31,
1903.

Newstead. On the Perivisceral Cavity of Ciona. Quart. Journ. Mic. Sc. , vol. 35,
1894.

Pizon. Observations sur le bourgeonnement de quelques Ascidies composees
(Didemnidae et Diplosomidae). Compte rendue Acad. Sc., 1891.

Pizon. L'Evolution des Diplosomes (Ascidies composees). Arch. zool. exp., series
4, vol. 4, 1905.

Hitter, W. Budding in Compound Ascidians based on Studies on Goodsiria and
Pcrophora. Journ. Morph., vol. 12, 1897.

Salensky. Neue Untersuchungen iiber die embryonale Entwicklung der Salpen.
Mitt. Zool. St. Neapel, vol. 3, 1883.

Salensky. Beitrage zur Entwicklungsgeschichte der Pyrosomen. Zool. Jahrb.
(Abt. f. and), vol. 4, 1891 ; vol. 5, 1894.

Schaxel. Die Morphologic des Euvachstums mid der Follikelbilduugen hei der
Ascidien. Ein Beitrag zur Frage der Chromidien bei Metazoen. Arch. Zellforsch.,
vol. 4, 1910.

De Selys-Longchamps. Etudes du developpement de la branchie chez Corella avee
line note sur la formation des protostigmates chez Ciona et Ascidiclla. Arch, biol.,
vol. 17, 1901.

De Selys - Longchamps and Damas. Recherches sur le developpement post-
embryonnaire et l'anatomie definitive de Mohjula ampulloides. Ibid.

Van Beneden and Julin. La Segmentation chez les Ascidiens dans ses rapports avec
rorgauisation de la larva. Arch, biol., vol. 5, 1884.

Van Beneden and Julin. Recherches sur la morphologic des Tuniciers. Ibid..
vol. 6, 1887.

Willey. Studies on the Protochordata. Quart. Journ. Mic. Sc., Pt. I., vol. 34,
1893 ; Pt, II., vol. 35, 1893.

CHAPTER XVIII
SUMMAEY

Ouu survey of the embryology of the Invertebrata is now completed,
but, before closing the volume, it seems desirable to pause for a
brief space and reflect, so that, if there are any general principles
to l>e deduced from the study of the series of life -histories which
have been described, they may not escape us.

The first and most far-reaching conclusion which we may draw,
is that, in general, the larval phase of development represents a
former condition of the adults of the stock to which it belongs.
This, in substance, is of course the recapitulatory theory of develop-
ment, the famous biogenetic law of Haeckel. In these days this
law is regarded with disfavour by many zoologists, so that to rank
oneself as a supporter of it is to be regarded as out-of-date. The
newest theory is, however, not necessarily the truest ; and this
we may certainly say, that if there has been evolutionary change
at all, which no one seriously doubts, — if every species of animal has
not been created, adapted 'to the conditions in which we now find it,—
then, nothing can be more certain than that the parasitic members
of the great natural groups are descended from ancestors which con-
formed in their structure to the normal type of the group in question.

Now, in the life-histories of these parasites, the larva, in almost
every case, shows an unmistakable resemblance to the normal type
of adult in the group. It appears to us that we have in such animals
a critical case by which we can test the truth of the recapitulatory
theory ; since, so far as human intelligence goes, the ancestry of such
creatures is known. Does any naturalist seriously doubt that the
ancestors of Adheres ambloplitis, described in Chapter VIII., were
once ordinary Copepoda ? As Metschnikoff has said, parasites are
really the latest products of evolution.

If, however, the recapitulation of ancestral structure turns out
to be the primary explanation of developmental history in cast's
where the ancestry is known, surely we have the right to assume that
the same type of explanation is valid where the ancestry is other-
wise unknown, and to conclude that in general the larval phase has a
recapitulatory significance.

049

650 INVERTEBRATA

CHAP.

Of course this conclusion was tacitly assumed by all evolutionary
zoologists thirty years ago, but few have paused to think what con-
sequences are implied in this conclusion. Among these few must be
reckoned Sedgwick (1909), who points out that on this theory it
follows that, as time goes on, the life-cycle must be ever tending to
grow more complex, since new phases are always being added to it
at its adult end. Another way of phrasing this conclusion is to say
that a new step in evolution usually takes place when the adults of a
species seek a new environment, and in reaction with it have their
structure modified.

If we inquire whether the adults of a species do often seek a
new environment, then some very interesting evidence may be
adduced. Allen (1899), as a result of several years' painstaking
exploration of that portion of the English Channel lying in the
neighbourhood of Plymouth Sound, has shown that each marine
species has a particular type of bottom which is suited to it, and
which may be termed its home. On ground of this kind it swarms;
but around the areas of this type of bottom numerous stragglers of
the species are to be found. It seems clear that, from the home
population, crowds of colonists are for ever being sent forth which,
in most cases, i'ail to maintain themselves, but which may in rare
cases successfully establish themselves, and in this way a new race
or species may be produced. Every species, indeed, can be compared
to a tire in the midst of a dry prairie, which for ever tends to extend
its borders.

IS'ow when an animal encounters a new environment one of two
tilings will result ; either its metabolism, and as a consequence all
its activities, will be checked ; or the metabolism will be promoted
and the vigour of its life increased. In the first case it will either
die or lead a stunted and sickly existence; in the second case its
structure will almost certainly be modified. This modification may
be described as a reaction to the stimulus of the new environment;
and as environment can be analysed into a few factors, such as food,
temperature, moisture, salinity, etc., the modification must, in the
last resort, be the effect of one or more of these on the metal lolism.
When, therefore, we find that the larva, as compared with the adult
ancestral stage which it represents, is almost always very much
reduced in size, and that the change to the adult condition takes
place whilst the animal is still very small, one receives the impression
that one is dealing with a reaction which, constantly repeated through
thousands, nay, myriads of generations, tends to set in sooner and
sooner in the course of the development ; just as in the life of the
individual, the formation of habit causes reactions to require for their
evocation less and less of the original stimulus.

But, the reader will exclaim with horror, does not this explana-
tion postulate the acceptance of that Larnarckian heresy, the inherit-
ance of acquired characters ? and have not experiments shown such
an idea to be devoid of foundation ? The answer to this question

xvm SUMMAEY 651

is twofold : first, the difficulty of framing any other theory of
recapitulation seems to be insuperable ; and, second, the experiments
which have been held to disprove the inheritance of acquired char-
acters are far from conclusive.

To take the first point first: If the chequered course of develop-
mental history is the result of the preservation of chance variations
in the struggle for existence, then we have to assume that, in the
eggs of animals living in one environment, variations occurred
which were suitable to new environments, and which manifested
themselves at the period of adolescence. That, to take a concrete
example, among the eggs of the Copepod ancestor of Act/ieres, some
varied so that at adolescence the organisms developed from them
tended to lose all their appendages, and that this loss had nothing
to do with the reaction to the new environment (gills of fish) in
which the animals found themselves. Or, to take another instance,
the hermit crab did not acquire its curved abdomen in consequence
of the habit of thrusting it into the empty shells of gastropod
molluscs; but since the curvature appears in these animals when they
are reared in confinement from the larval stage and prevented from
finding shells at all (Thomson, 1904), we must assume that in this
species the tail became curved in the proper spiral by chance varia-
tions, and that then its possessor formed the useful habit of seeking
gastropod shells to clothe it. Such explanations are perhaps not im-
possible, but, to speak frankly, they do not commend themselves
to us.

To consider now the second objection. The evidence from
experiments is not at all conclusive. The earlier experiments
designed to test the inheritability of acquired characters, can only
be described as childish. They consisted in such things as cutting
off the tails of mice, and in rearing the offspring of these mutilated
animals, in the expectation that the young would be born without tails.
If any thing acquired can be inherited it must surely be some reaction
of the organism as a whole. Now Kammerer (1913) has shown that,
by keeping salamanders for several generations in certain environ-
ments marked changes in skin coloration result ; and that, after a
time, not only do the beginnings of these changes show themselves
in the young before they are exposed to the new environment, but
these altered forms, when crossed with the original forms, behave
like Mendelian races (see Chapter I.).

It must be remembered that the experiments of the Mendelian
school of biologists, which are held to demonstrate the unalterable
character of the reproductive substance or germ-plasm, have bcvn
continued through only a very few generations ; whilst to obtain
the inheritance of acquired characters the action of the new environ-
ment would probably, in most cases, be continued through thousands
of generations. The evidence from Palaeontology seems to suggest
that, in making structural advances, Nature acts with extreme
slowness. It required the whole length of the Secondary Period to

652 INVEETEBKATA CHAP.

make a crab out of a lobster-like ancestor, and the whole of the
Tertiary Period to convert a five-toed mammal into a horse.1

The. dislike with which the Lamarckian theory is viewed is not
entirely due to the supposed evidence against it furnished by experi-
ments. Two other considerations have been urged : first, that there
are modifications which cannot have been the result of the inheritance
of acquired characters ; and, second, that it is difficult to conceive of
any mechanism by which the characters of the body can be transferred
to the germ.

In the first objection there lurks some confusion of thought. It
is tacitly assumed that acquired characters must be changes of
structure due to new habits acquired by the animal in adaptation to
its new environment. But to assume this is to narrow, in an
unwarrantable fashion, our conception of what constitutes an acquired
character. The reaction to the environment need not be an adapta-
tion. Certainly it will only be preserved if it happens to lie an
adaptation, or if it is at least not harmful. But even with this
widening we must admit the justice of Lankester's criticism of such
explanations, as applied to the habits of insects in feigning death :
" An insect either postures and escapes, or it does not posture and it
is eaten ; it is not half-eaten and left to benefit from experience."

But our aim is not to explain the origin of all specific differences
—it is the much more modest one of attempting to give a rational
account of recapitulation.

As to the second consideration which is urged against the inherit-
ance of acquired characters, viz. the difference of forming a conception
of its modus operandi ; its great weight muse be admitted, but even
here we are beginning to receive light from both physiology and the
new science of experimental embryology. The discovery of hormones,
by Starling, is of far-reaching importance in this respect. These are
substances, produced by certain organs of the body and poured into
the body -fluids, which have a powerful effect on growth and other
metabolic processes. Now, it is quite possible and even probable
that the few hormones which so far have been discovered, such as the
hormones of the thyroid and pituitary glands, have been recognized
on account of their exceptionally active chemical character, and that
hormones of lesser strength are given off by all the tissues of the
body, and that the various organs of the body stand in a sort of mobile
chemical equilibrium with one another.

Consideral >le support can be drawn from experimental embry ol< >gy
in support of this view. Herbst (1899) has shown that if the eye of

1 Since these lines were written an interesting example of the stereotyping of a
functional reaction has occurred to us. In the lagoons of Prince Edward Island,
where the oyster swarms, two varieties occur : one, the so-called Cup-oyster, on hard
shelly or gravelly ground ; the other, the Mud-oyster, on mud. In the latter the
edges of both valves are curved up so as to keep the opening above the mud ; in the
other the edges of the valves remain horizontal. Both varieties develop from the
same larvae. Now in secondary strata there occurs a genus, Gryphaea, which is just
a Mud-oyster stereotyped, and it is found in clay deposits.

xviii SUMMARY 653

the shrimp be cut out, a new eye will be regenerated so long as the
optic ganglion is left intact, but that it' the optic ganglion be cut out,
an antenna-like organ will lie regenerated instead. The only possible
explanation of this fact is to conclude that some influence — a hormone,
in fact — emanates from the optic ganglion, which so influences the
regenerating ectoderm as to determine that it shall take on the
extremely complicated structure of the compound eye.

A still more striking case has been described by us (MacBride,
1911). In the development of the ordinary sea-urchin normally only
one water -vascular rudiment or hydrocoele is formed, and this is
situated on the left side of the larva. The ectoderm lying above it
becomes iuvaginated to form a deep sac — the amniotic sac. From
the floor of this sac are developed the adult nerve-ring and adult
spines. In the centre of the floor an invaginatiou is formed which
gives rise to the adult mouth. From the peritoneal epithelium of
the left coelomic sac, which lies beneath the hydrocoele, are developed
the dental pockets and the teeth which project into them.

But occasionally a second hydrocoele is developed which is
situated on the right side of the larva. When this takes place the
ectoderm on the right side of the body becomes invaginated to form a
deep sac, from the floor of which a second nerve ring, a second set of
adult spines, and a second mouth are developed, whilst the underlying
peritoneal epithelium of the right coelomic sac gives rise to a second
set of dental pockets.

Now, although we have good reason to believe that the common
free-swimming ancestor of all Echinoderms possessed two hydrocoeles,
yet it is as certain as anything can lie that this ancestor did not
possess two mouths surrounded by nerve rings, nor did it have the
highly differentiated opines and teeth of the Echinoid. The production
of a second hydrocoele is probably an ancestral reminiscence, but the
production of these other organs cannot possibly be so explained.

The only conclusion, therefore, that we can draw is that, in the
natural development of >Uchi?t,us, the hydrocoele emits a hormone
which causes the ectoderm to form the amniotic invagination, and
which causes the left coelomic vesicle to give rise to the dental pockets.
It follows further, that particular portions of ectoderm and of coelomic
wall are not specialized so that they alone can undergo these modi-
fications, but that any portion of the ectoderm and any portion of the
coelomic wall can undergo similar modifications, provided that they
are acted on by the appropriate hormone, as is shown by the effect of
the right hydrocoele on the right coelomic sac and on the ectoderm of
the right side. Development then is a kind of progressive specializa-
tion, due to the influence of one organ on another by means of
hormones.

Professor Langley has pointed out to us (in, literis] that if an
animal changes its structure in response to a changed environment
the hormones produced by the altered organs will be changed. Tin-
altered hormones will circulate in the blood and bathe the growing and

654 INVERTEBKATA CHAP.

maturing genital cells. Sooner or later we may fairly assume that some
of these hormones may become incorporated in the nuclear matter of
the genital cells ; and then, when these cells develop into embryos, the
hormones are set free at the corresponding period of development to
that at which they were originally formed. They reinforce the action
of the environment and cause it to produce greater effects ; they
may become free even before the stimulus of the environment reaches
them, and produce the appropriate structural change at an earlier
period of development. In this way we explain the tendency not only to
recapitulate, but to reflect back ancestral structures into progressively
earlier periods of development.

We do not assume for a moment that this is a full and satisfactory
explanation of recapitulation, we regard it merely as a sketch of the
direction in which the explanation may be found, and as a call for
further investigation.

But recapitulation of ancestral structure is by no means the only
factor in development ; and we must now inquire whether our studies
have led us to form an idea of what the other factors are. One has
been already alluded to, viz. the tendency for changes in structure to
make their appearance in successively earlier periods of growth, and
consequently for the larva to be reduced in size. That this reduction
in size entails changes in the larval organs has already been pointed
out. We have seen that serially repeated organs, like the legs of the
Nauplius, may be reduced to two or three pairs of those which are
functionally the most important ; that organs which should occur in
pairs, arranged in a bilaterally symmetrical manner, may be repre-
sented by one-sided structures, such as the eye of the Ascidian tadpole
and the " primary " gill-slits of Ampliioxus.

Even here the researches of experimental embryologists may aid
us. Driesch (1900, 1910) has succeeded in inducing two or three
early larvae of Echinus to fuse into a single compound organism.
This compound larva naturally possessed three guts, but one only
grew large and became functional, the others dwindled, no doubt
owing to some inhibiting influence on their growth emitted by the
larger one. So we may imagine that larval organs which are
functionally necessary, and which increase, owing to their use, out of
all proportion to the proportion they should sustain to the organism
in which they find themselves, must inhibit the growth of their less
fortunate sisters.

Again, we must remember that whilst the reaction to the final
environment has evoked and sustains the adult structure, the larva
has also its environment. Whilst in many, nay most cases, we have
reason to believe that the larval environment has the same general
characters as the environment of the ancestral stage which the larva
represents, yet in no case is it probable that the two environments
are exactly alike, and in some cases the larval environment has
become markedly different from what the ancestral one must have
been.

XVIII

SUMMARY (555

Even the reduced size of the larva and the tendency for adult
organs to develop precociously will alter its relation to the environ-
ment. The enormously long ciliated arms of the Ophiopluteus larva
are necessary to sustain the growing weight of adult calcareous plates
which make their appearance in the later stages of larval life. The
free-swimming ancestor represented 1 >y the larva had almost certainly
no calcareous plates at all.

When, as in the case of insects among Arthropoda, and Unionidae
amongst Mollusca, the larvae take to special modes of life, the modi-
fications of the recapitulatory history become profound, and special
larval organs are produced ; such as the tracheal gills of the nymphs
of Ephemeridae, or the hooked apices of the shell-valves in the
Glochidium larva, which never existed as organs in any adult
ancestor, and whose presence may lie regarded as a falsification of
embryonic history.

If it be asked how these secondary characters are to be dis-
criminated from primary larval characters, the answer is that primary
larval characters connect different groups of the animal kingdom,
such as the organs of the Trochophore found in almost identical form
in Mollusca, Annelida, and Polyzoa ; or the Nauplius larva found in
Phyllopoda, Copepoda, Cirripedia, and Malacostraca. Secondary larval
characters are confined to stnallet groups, and sometimes betray their
secondary character by their peculiar structure. Thus the tracheal
gills, alluded to above, allow the oxygen dissolved in the circumambient
water to come into proximity, not with blood contained in these gills as
in all other gills, but with air contained in them, from which in turn
the blood derives its oxygen. Here is the clearest indication that in
the ancestral stock the larva was originally air-breathing in habit
and took to water as a shelter.

But we have learnt to recognize yet another modifying factor in
development. As the race progresses in evolution and successively
seeks new environments, there will be a tendency to leave behind it a
trail of larval stages representing past conditions of the stock. In
some cases, as in the life-history of Penaeus, at least four successive
larval stages can be recognized. But in each larval stage the species
is exposed to special dangers and suffers enormous mortality. If
therefore the earlier larval stages can be passed through either within
the mother's body or inside an egg-shell, this mortality will be greatly
lessened.

This change has taken place to some extent in all life-histories,
for every life-history starts with an embryonic phase. In some lift--
histories almost the whole of the development takes place under
shelter, and the young animal steps out into the world ready to take
up the adult mode of life. Such life-histories are said to be of tin-
embryonic type. They are so advantageous from the point of view
of infant mortality that the wonder is that any life-histories remain
in which the larval phase is predominant.

We must believe that the advantage to the race which the wide

656 INVERTEBEATA CHAP.

dispersion, resulting from the existence of a free-swimming larval
phase, confers on it, counterbalances the disadvantage resulting from
the mortality of the larvae. Generally speaking, the more modified
and more advanced in structure a species is, the more prominent is
the embryonic phase in its life-history. But in isolated cases, within
each natural group of animals, almost the whole of the life-history
may become embryonic, whilst the adult structure remains compara-
tively unmodified. So we find that in Peripatus capensis, one of the
most primitive of Arthropods, the whole of the development is passed
within the maternal oviduct ; and that in Amphiura squamata the
young emerges from the genital bursa of the mother as a perfect brittle-
star, whilst nearly allied species have a long larval development.
Such cases could be multiplied, and there can usually be found some
reason in the peculiar local conditions of the species which makes a
larval life peculiarly dangerous.

But even when larval life has begun, its even course is sometimes
interrupted by phases which we may term pupal, and which show a
striking similarity to embryonic phases. During these the growing
form may shelter itself in some kind of case, either of extraneous
matter or of its own secretions, and takes no food, whilst extensive
internal changes go on. In less marked pupal stages the creature
continues to lead a free life but takes no food. We may recall to the
reader's mind the pupal stages of Cirripedes and Holothuroids.

The reason for these modifications is clear. In every larval stage,
as we have seen, the creature encounters dangers and has a special
way of obtaining food. In one and the same locality these different
ways are probably not equally effective. It is therefore a great
advantage if enough food can be accumulated during one larval stage
to enable the next to be passed rapidly through without needing food
at all. The most common form of this is to find that the larvae, when
just hatched, retains a store of food in its tissues from the preceding
embryonic stage, and whilst it moves about freely it requires no food.
The yolky larvae of Asterina, Cribrella, and Solaster, among brittle-
stars, may be mentioned, as also of most Ectoproct Polyzoa. Such
creatures are really intermediate in type between embryos and larvae.

Finally, in rare cases, the alteration of conditions, either of climate
or of the nature of competitors, may cause the larval stage to become
more safe and advantageous than the adult ; and in this case the
adult stage is employed only for pairing and egg-laying, and is passed
quickly through, or it may be suppressed altogether. Originally the
conditions of adult life must have been more advantageous than those
of the larva, or the evolutionary step from the one to the other would
never have been taken. But we have already pointed out that the
imagiual stage in many of the higher insects is of very short durati< >n,
and that during this stage, in many cases, no food is taken ; and here
we must assume that the life of the larva is less dangerous than that
of the adult. Again, among some Urodeles, such as the Axolotl, the
larva can develop ripe genital organs whilst continuing the larval

xvni SUMMARY 657

mode of life, and then the adult stage, for the evocation of which the
appropriate stimulus has ceased, drops out. As is well known, this
lust adult stage can be evoked in the Axolotl when the proper
stimulus is discovered and artificially applied.

From considerations of the secondary factors which modify larval
life, we pass to the factors which modify embryonic Hie. Of these
the most important is food. Food is supplied to the embryo either
in the form of yolk grains embedded in the cytoplasm of the egg, or
of maternal secretions. These two forms of food give rise to different
kinds of modifications. To take the yolk first. Its presence in any
quantity slows down cell division, as Balfour (1881) has pointed out,
and in extreme cases abolishes it altogether, leaving only division of
nuclei. It causes the number of cells produced to be smaller, and the
size of the individual cell to be larger, and so it renders such processes
as the formation of pouches, or of folding, impossible, and they are
replaced in the yolky embryo by processes of solid proliferation of
cells. Ordinarily speaking, yolk is stored in the cells which will
afterwards form part of the gut, but in certain cases, as in certain
Ecliinoderm embryos, it is more widely distributed; and then the
most profound modification in early development can take place, the
whole of the archenteric wall may be directly converted into coelom,
and the true gut formed later as an outgrowth from this.

Maternal secretions are in most cases absorbed through the
ectoderm, and the effects of this change of function on this layer are
profound. The extraordinary spongy ectoderm of Peripatus capensis
is due to this, but the most striking instances of the effects of this
kind of food on the development of the embryo are found amongst
Mammalia, and will doubtless be dealt with in the third volume of
this work.

Finally, it must be remembered that, in the embryonic phase
of development, the functional correlation of the development of
the various organs necessary to the larva, as to every free-living self-
-supporting organism, can be profoundly altered without impairing the
end of development — viz. the successful attainment of the adult form.
The structure of the embryo, at any period, is the outward and visible
expression of the co-working of independent processes, held together
by a very loose rein. A beautiful instance of this has been given by
Jeukinson (1906). In the embryo of Urodela the lower part of the
blastopore remains continuously open and eventually forms the anus.
In the Aiiurau embryo this part of the blastopore closes, but the anus
is formed later as a new perforation in identically the same place.
Now, by allowing the Anurart egg to develop in solutions of certain
salts, the blastopore can be caused to remain open and the egg then
develops after the Urodele manner. The question as to whether the
blastopore persists or not is, therefore, merely a question of the value
of the differential equation connecting the rates of growth of the
archenteric walls, and the rate of expansion of the archenteric
cavity.

VOL. i 2 u

658 INVERTEBRATA CHAP.

Speaking of the geological record, Darwin wrote, in 1859, that of
the hook of life we only possess the last volume. This conclusion, so
far as Invertehrates are concerned, has been amply confirmed hy the
remarkable discovery by Walcott (1912), of a richly differentiated
and exquisitely preserved fauna in the Mid-Cambrian rocks of North
America. If therefore the relationship to one another, not only of
the various phyla of the animal kingdom, but even of the classes
within the phyla, is ever to be elucidated, it can only be done by
Comparative Embryology. Palaeontology begins too late to undertake
the task.

From all the discussion, however, which has just been completed,
of the secondary factors which modify the recapitulatory record in
both embryonic and larval life, it will be clear that only an Embryology
based on an enormous collection of facts, and a careful comparison of
one type with another, can hope to discriminate between primary and
secondary factors in development, and to elucidate ancestral history.

It is because too many zoologists have based far-reaching theories
on the life-history of some one type, that recapitulatory embryology
has fallen into bad repute. But the remedy for the abuse of little
light is more light, and already, by the steady accumulation of
embryological data and the improvement of methods, some of the
controversies which vexed our fathers in the 'eighties are in a fair
way to be settled.

The late Professor Welldon pointed out that it would be of great
interest and importance to find out how far the most recent evolu-
tionary changes, such as those which made the difference between
genera within a family, and between families within a tribe, are
represented in the life-history. Here is a field for research of great
importance, in which very little work has as yet been done. These
latest stages of the life-history should be the freest from disturbance
by secondary factors, but it is precisely over the interpretation of the
earliest stages in the life-history, which represent the oldest pages in
the ancestral record, and which one would expect to be most blurred,
that the greatest disputes have arisen.

There is a school of embryologists, led by Driesch, who decry the
value of the recapitulatory interpretation altogether, and who insist
that the developmental processes of every animal should he referred
back to causes existing in its egg, and that no hypothetical ancestry
should be called in to aid in the explanation. No doubt it is true,
theoretically, that the stages in the development of an animal form a
continuous series, and that the causes for the production of each
stage are to be found in the preceding one. But even if this causal
chain were completely elucidated, it would leave entirely unexplained
the marvellous resemblances between the larvae of some species and
the adult stages of others, or between the larvae of widely different
groups ; and it is precisely phenomena of this kind that Comparative
Embryology seeks to account for.

In this search Comparative Embryology has been very greatly

xvm SUMMARY 659

aided by the science of Experimental Embryology, founded by Koux,
and so ardently followed by Driesch, Herbst, and many others. If we
ask ourselves what is the most remarkable achievement of this science,
the answer must surely be the discovery of organ-forming substances.
We have already pointed out that such substances are emitted by the
nucleus of the ripening egg into the cytoplasm, and that they confer
on the latter a definite character ; and that the early course of develop-
ment consists in separating these substances from one another, and in
allocating them to different regions of the segmenting egg and embryo.
This separation can occur at an earlier period in one type of egg
(Annelida, Mollusca, Ctenophora, Tunicata), and at a much later period
in another type of egg (Hydrozoa, Echinodermata). Until it has been
effected a portion of the egg will produce a perfect embryo of
reduced size.

We now see the inner meaning of that much debated " formation
of the layers," over which so many battles have been fought. Pressure
experiments prove abundantly that, after the primary emission of
organ-forming substances, the nuclei of the developing embryo form
an indifferent material, and what settles the fate of any cell is the
quality of the organ-forming substance locked up in it. But, as we
have already pointed out, this indifference of the nuclei is a passing
phase, because, for one tiling, if it were permanent, the male pro-
nucleus brought in by the spermatozoon would have no effect in
determining development, which is notoriously not the case. The
later course of development may be regarded as a result of the action
of already-formed organs on one another by the aid of hormones.
But indeed the organ-forming substances themselves are most plausibly
regarded as of the nature of hormones or ferments. This is clear from
the consideration that the quantity of the organ-forming substance
can vary within wide limits and yet give rise to a perfect organ. A
certain minimal quantity in the fragment of an egg will lead to
precisely the same result as a much larger quantity (cf. Boveri's
experiments on the eggs of Ascaris, Chap. XV.).

We cannot for a moment imagine that the molecules of the organ-
forming substance are little pictures of the organ which it is their
function to produce. Of course it is a mere commonplace to say that
we are only on the threshold of our knowledge of these substances,
and are still very far from understanding their modus operandi.
How is it, for instance, that a slight prick with a knife in the bud
from which a new tail is regenerated in a lizard which has lost its
tail, is capable of bringing it about that two tails, and not one, are
developed ? So far as our knowledge goes, it seems to be clear that
for the formation of an organ of what we may call the second order
(i.e. such a thing as a head or a limb), as distinguished from an organ
of the first order, or a germinal layer, the co-operation of at least two
organ-forming substances, in definite spatial relations to each other, is
necessary.

If the spatial relations lie altered we may get two organs formed

660 INVERTEBRATA CHAP.

by the co-operation of the substances, instead of one. If, for instance,
the 2-cell stage of a developing frog's egg be compressed between
two glass slides so that it cannot rotate as a whole, and the prepara-
tion inverted, a double-headed tadpole will result. Here nothing has
been removed, nor have the connections of the blastomeres with each
other been destroyed, but the spatial relations of the organ-forming
substances have been altered under the influence of gravity, and as a
result the tadpole has two heads instead of one. 01 a quite similar
nature are the results obtained by Spemann (1901, 1903) on the
gastrula of the newt, when he employed constriction by a string, and
a two-headed monster resulted. So much we can determine empiric-
ally, but the how and why are still to seek.

The reader will see that the door is opened to a host of interesting
questions, and that indeed experimental embryology passes into
cytology, for the whole question of the relation of the nucleus to the
cytoplasm is raised. To take one example of such questions, we may
ask, if the nuclei of the segmenting egg are indifferent material, and
the distribution of cytoplasmic organ -forming substances is fixed at
the moment of fertilization, and if these substances, as seems certain,
are of purely maternal origin, at what point in development does
the male influence assert itself? For this point must coincide with
the point of renewed nuclear activity. A series of carefully chosen
hybridization experiments should throw light on this problem.

Again, we have seen reason to ascribe the formation of buds to
the reassumption of an active role on the part of the nuclei of adult
tissue, and the renewed formation of organ-forming substances. We
have ascribed the different course of the development of buds from
that obtaining in embryonic development to a different distribution
of these substances. Can we detect microscopically any difference
between these active nuclei and the normal inactive nuclei ? Here
again is a fruitful field for research.

Let us in the meantime, adopting the recapitulatory view,
provisionally sketch the developmental history of invertebrates so far
as our present knowledge extends.

In the larval history of the least modified Sponges, Coelenterata,
and Echiiiodermata — groups which, in the differentiation of their adult
organs, are the lowliest amongst Invertebrates — the first distinct
larval phase is the blastula, which is a hollow sphere or ellipsoid,
whose walls are constituted by a single layer of flagellated cells.
Since this larval phase is represented in a form more or less obscured
by secondary changes in the embryonic life-history of all the other
groups, we may take it as representing in rudest outline the form of
the common ancestor of all Metazoa. It resembles in many respects
certain existing colonial Protista, such as Volvox, sometimes claimed
by zoologists and sometimes by botanists.

Such a simple, free-swimming stock must have swarmed in the
shallow, warm seas of the primitive globe, when there were no higher
forms to compete with it. At first every cell fed itself like every

xviii SUMMARY 661

other, but later, when some members of this widespread stock took to
a creeping life, then the lower cells, in contact with the nutritive
substratum, remained nutritive, but the upper cells became protective,
and formed a covering dermal layer ; and so the group of Sponges or
Porifera were evolved.

In those members of the stock which remained free-swimming,
however, the direction of progression changed from an indefinite
rotation to a definitely directed progress ; the hinder cells became
adapted to catch nutriment, the anterior became purely sensory.
The nutritive cells became increased in number and invaginated, and
so the primary gut was formed, and the stock were no longer blastulae
but gastrulae.

The gastrula stage exists as a larval phase in more cases than
does the blastula one, and it is likewise represented, in obscured form,
in the embryonic history of the higher types. Some of the gastrula
stock likewise took to a bottom life, and gave rise to the Hydrozoa,
Scyphozoa, and Actinozoa, amongst Coelenterata.

The main portion of the stock remained, however, free-swimming,
and developed lateral pouches of the gut, in which excretory and
reproductive functions were specialized, and which also gave rise to
cells of a specially locomotor character ; while at the aboral pole the
sensitive cells had become a definite nerve centre.

In this way a primitive wide - ranging group was evolved,
supplanting the gastrula stock, to which we may give the term
Protocoelomata. In much modified and specialized form this stock
survives as the Ctenophora at the present day. But the Proto-
coelomate stage in the development of the race is represented in the
ontogeny of Invertebrata by three distinct types of larvae, viz. the
Trochophore larva, the Echinoderm larva, and the Tornaria larva. The
latter two types of larva probably do represent the same type of
ancestor, but the Trochophore larva, with its early specialized develop-
ment, is different ; it is more closely allied to existing Ctenophora,
and the coexistence of these two types points to the existence of
different types of specialization amongst the original Protocoelomate
stock. The Brachiopod larva is in many ways intermediate in
character between the two types.

From the division of Protocoelomata represented by the Trocho-
phore, bottom-living forms were produced. These, as we have pointed
out in the proper place, are the burrowing Annelida, the creeping and
gliding Mollusca, as well as Podaxonia, and Ectoproct and Entoproct
Polyzoa. The Nemertinea are also bottom-haunting forms descended
from the same stock. The Platyhelminthes represent an earlier off-
shoot from the Trochophore stock, before the primitive mouth had
been cut into definite mouth and anus, and the lateral branches of
the gut definitely specialized as coelom. The Brachiopoda are a
bottom-living group, descended from a type of Protocoelomata inter-
mediate between the Ctenophore-like ancestor presented by the
Trochophore larva and the Dipleurula ancestor of Echinodermata.

662 INVEETEBEATA CHAP.

From the Annelida arose Arthropoda, whose members in some
degree regained the free -swimming life of their far-off ancestors ; but
they never regained domination in the open sea, for, in the meantime,
that portion of the Protocoelomate stock represented by the Dipleurula
had advanced in development, developing long ciliated tentacles
for the prehension of food ; and this section of the stock leads
straight on to the victorious Vertebrata, whose leading members
have never deserted the free life of the ocean rover, and have been
and are now dominant in the seas.

From time to time weaker brethren have given up the struggle
and sought safety in a bottom life; of these the oldest offshoot are
the Echinodermata, later came the Cephalodiscida, and then the
Balanoglossida, which, though classed together as Enteropneusta,
represent two separate offshoots from the free - swimming Proto-
coelomata. Then, much later, the Cephalochorda diverged, later still
the Urochorda (Tunicata), and finally the Cyclostome Fishes.

It is, therefore, broadly speaking, true that Invertebrates collect-
ively represent those 1 tranches of the Vertebrate stock which, at
various times, have deserted their high vocation and fallen to lowlier
habits of life.

When once a stock has so fallen, is there a place for repentance ?
Can a dominant position lie regained ? At first sight the history of
Arthropoda appears to answer this question in the affirmative, for they
have certainly progressed far beyond their Annelidan ancestors. As
all know, vigorous attempts have been made to prove that Vertebrata
are evolved" from Arthropoda. The only evidence for this is the
superficial similarity between certain early Arachnida and fossil
Fishes, coupled with the assertion that Arthropoda were dominant
in the seas before Vertebrata, and that a dominant group like
the Vertebrata must have arisen from a pre-existing dominant
group.

Now the difficulty in the way of this view, even supposing that the
enormous differences between vertebrate and arachnid anatomy could
be brushed aside, is that the fish which are compared to Arachnida are
degenerate bottom-living forms. They are not the earliest and most
primitive fish, whose blade-like bodies swept like arrows through the
waters above. The Arachnida, with which they are compared, are
also almost certainly bottom-living forms, and there is no evidence
that the Arthropoda, except in the case of minute-bodied incon-
spicuous forms, such as Copepoda and Cladocera, ever really took to
active life in the open sea again. The larger and heavier types are
all bottom -living, and it seems perfectly clear that, when the
Arthropoda sought to recover their lost birthright, they found the
ground preoccupied by the Vertebrata and their opportunity gone
for ever.

In adaptation to life on land, however, Arthropoda were beforehand
with their rivals, and in pre-Carboniferous days must have expanded
and flourished enormously; but the start was speedily overhauled^when,

xvni SUMMAKY 663

in Carboniferous days, the Vertebrata followed them on to land and,
though as Insecta the Arthropoda still maintain themselves and limit
the activities of land Vertebrata in many ways, yet if we have regard
to bulk of body, and above all to ps}rchic development, there can be.
no question as to which is really the victorious race.

Our task is finished ; we have striven to represent the science of
Comparative Embryology, not as a well-ordered and complete system
of philosophy, but rather as a gold-mine from which rich rewards have
already been reaped, but of which only a small part has as yet been
developed, and which promises abundance of gratifying surprises and
rewarding returns to the worker of the future.

" The harvest truly is plenteous, Init the labourers are few."

LITERATURE REFERRED TO

Allen. On the Fauna and Bottom-deposits near the 30-fathom line from Eddystone
Grounds to Start Point. Journ. Mar. Biol. Ass., vol. 5, 1899.

Balfour. Text-book of Comparative Embryology, vol. 1, 1881.

Darwin. Origin of Species. First Edition, 1859.

Driesch. Studien iiber die Regulationsvermogen der Organismen bei Echiniden-
keimen. No. 4, Die Verschmelzuug der Individualitat. Arch. Ent. Mech. vol. 10, 1900.

Driesch. Neue Versuche iiber die Entwicklung verschmelzenen Echinidenkeime.
Ibid. vo'l. 30, 1910.

Herbst. fiber die Regeneration von Antennen-ahnlichen an Stelle von Augen.
Arch. Ent. Mech., vol. 9, 1899.

Jenkinson. On the Effect of certain Solutions upon the Development of the Frog's
Egg. Ibid. vol. 21, 1906.

Katnmerer. Vererbung erzwungener Farbveranderungen. No. 4, Das Farbekleid
des Feuer-Salamanders (Salamander maculae). Ibid. vol. 36, 1913.

MacBride. Two abnormal Plntei of Echinus and the Light which they throw on the
Factors in the normal Development of Echinus. Quart. Journ. Mic. Sci., vol. 57, 1911.

Sedgwick. The Influence of Darwin on the Study of Animal Embryology. [Darwin
and Modern Science.] Cambridge, 1909.

Spemann. Entwicklungsphysiologische Studien am Triton-Ei. I. Arch. Ent.
Mech. vol. 12, 1901; II. Ibid. vol. 15, 1903 ; III. Ibid. vol. 16, 1903.

Thompson. The Metamorphoses of the Hermit-crab. Proc. Boston Soc. Nat. Hist.,
vol. 31, 1904.

Walcott. Middle-Cambrian Branchiopoda, Malacostraca, Tiilobitaand Merostomata.
Smithsonian Miscellaneous Collections, vol. 57, No. 6, 1912.

INDEX OF AUTHORS

f.B. — Figures printed in heavy type indicate that the Author's name occurs on these
particular pages in the lists of " Literature consulted."

Agar, 4, 12, 16, 31
Agassiz, 466, 566
Allen, 131, 650, 663
Alliiian, 74, 100
Appellof, 76, 81, 82, 83,
100

Balibur, 185, 204, 210, 217,

221, 288, C06, 647, 657,

663
Bateson, 16, 31, 569, 570,

581, 582, 583, 584, 647
Beecher, 238, 289
Beneden, Van, 609, 638,

648

Bergh, 157, 168
Bigelow, 194, 288
Born, 17, 31
Boutan, 300, 304, 370
Boveri, 439, 444, 451, 452,

453, 454, 455, 506, 566,

600, 647, 659
Brauer, 54, 55, 58, 100, 239,

240, 241, 244, 289
Brooks, 177, 191, 288, 416
Buchner, 429, 435, 436
Burger, 118, 127, 157, 168
Bury, 477, 516, 529, 533,

536, 544, 545, 566, 567
Biitschli, 428, 436

Caldwell, 381, 382, 383, 384,
385

Caiman, 218, 288

Carlgren, 85, 100

Carpenter, 544, 556, 567

Cary, 84, 100

Casteel, 321, 370

Castle, 616, 647

Cerfontaine, 586, 587, 588,
589, 647

Child, 129, 168

Chun, 66, 89, 94, 98, 100

Clarke, 529, 539, 567

Claus, 196, 197, 200, 210,
288

Conklin, 11, 31, 291, 370,
407, 408, 411, 413, 415,
417, 435, 451, 609, 610,
614, 619, 630, 631, 648

Crampton, 332, 370

Czwiklitzer, 386, 401, 406

Dalyell, 70, 100

Damas, 626, 628, 632, 648

Darwin, 18, 21, '23, 31, 657,

663
Davis, 570, 582, 583, 605,

647

Del age, 464
Delap, 472, 566
De Morgan, 523, 567
Dendy, 37, 38, 39, 47, 52
Dohrn, 210, 288
Doncaster, 428, 429, 434,

435, 436

Drew, 348, 349, 369, 370
Driesch, 20, 21, 29, 30, 31,

89, 96, 97, 98, 100, 451,

466, 483, 506, 524, 525,
526, 528, 567, 651, 658,
663

Drummond, 310, 316, 317,

370

Duerden, 84, 100
Duesberg, 7, 31

Eisig, 156, 168

Erlanger, 243, 289, 310, 311,

313, 318, 323, 370, 383,

415
Evans, 47, 52

Faurot, 85, 100

Faussek, 356, 365, 370

Fechuer, 628, 648

Fewkes, 499, 566

Field, 457, 461, 465, 466,

467, 566

Fischel, 89, 96, 97, 98,

100

Fraipont, 144, 168
Friedemann, 67, 70, 72, 100
Fnchs, 523, 567

Gardiner, 81, 100, 408
Gemmill, 457, 461,464, 466,

467, 469, 471, 472, 475,

481, 482, 566
Gerould, 373, 380, 385
Godlewski, 17, 31, 523, 567
Goldschmidt, 599, 647
Goodrich, 157, 159, 167, 168,

323, 381, 382, 385, 596,

600, 647

665

Goto, 457, 458, 467, 469,

475, 477, 566
Gntte, 57, 61, 62, 63, 64,

100
Grave, 501, 502, 503, 522,

566

Groom, 194, 288
Giinther, 273, 276, 289, 435,

436

Haeckel, 66, 100, 649

Harm, 62, 100

Harmer, 386, 395, 398, 402,

406
Harms, 312, 351, 352, 353,

370
Hatschek, 204, 288, 348,

349, 370, 380, 385, 398,

399, 401, 405, 406, 586,

589, 599, 647
Hazen, 591, 647
Heath, 320, 370
Heathcote, 284, 290
Heider, 64, 66, 99, 100, 204,

289, 386, 406, 570, 571,
574, 575, 582, 584, 605,
647

Hein, 67, 70, 73, 100
Herbst, 18, 29, 30, 31, 306,

370, 466, 483, 484, 525,

526, 527, 567, 652, 658,

663
Hertwig, 13, 31, 428, 435,

436, 439, 455
Heymons, 262, 263, 265,

266, 281, 282, 283, 289,

290, 324, 370
Hickson, Sti, 100
Hirschler, 245, 217, 249,

250, 253, 255, 256, 257,
260, 261, 262, 289

H.JMi-t, 635, 637, 638, 640,
'644, 648

Holmes, 324, 370

Horst, 348, 349, 370

Huxley, 53, 100, 242. 427

Hyatt. 19

Ik. 'da, 381, 382, 385

kiii-"ii. ''">7, 663
Jennings, I Is, 427

666

INVERTEBRATA

Julin, 609, 632, 633, 635,
638, 640, 648

Kammerer, 651, 663
Kautsch, 221, 223, 226, 228,

231, 235, 289
Keeble, 103, 117
Kerr, 319, 460
Kingsley, 221, 236, 289
Kishinouye, 221, 222, 2i>3,

224, 226, 235, 236, 240,

244, 282, 289
Koch, von, 86, 87, 100,

101

Koepperu, 354, 370
Korschelt, 64, 66, 99, 100,

204, 289, 356, 370, 386,

406
Kowalev.sky, 278, 289, 320,

370, 407, 416, 417, 428,

435, 436, 586, 589, 606,

608, 619, 647, 648
Kiilin, 193, 194, 289, 626,

648
Kupelwieser, 17, 31, 387,

391, 392, 405, 406, 523,

567

Lacaze - Duthiers, 87, 101,

329, 407, 417
Lamarck, 23
Lang, 103, 109, 112, 115,

116, 117
Langley, 653
Lankester, 46, 357, 369,

370, 372, 380, 385, 406,

407, 417, 584, 596, 608,

647, 652
Lebedinsky, 398, 401, 405,

406

Legro.s, 586, 647
Lillie, 333, 351, 353, 370
Lister, 216, 289
Loeb, 9, 17, 18, 29, 30, 31,

458, 523, 524, 567
Loven, 348, 371
Liulwig, 458, 477, 499, 534,

541, 542, 566, 567
Lwoff, 586, 589, 647

Maas, 43, 44, 46, 51, 52
MacBride, 472, 500, 504,

566, 567, 607, 647, 653,

663

Marshall, 50, 52
Masterman, 381, 382, 383,

385, 481, 566
Mazzarelli, 324, 371
McCluny, 13
McMurrich, 85, 101
Mcisenheimer, 312, 332, 333,

334, 335, 337, 338, 340,

348, 371
Mendel, 16

Metschnikoff, 59,
101, 122, 127,
381, 385, 533,
567, 569, 647,
Meyer, 165, 168
Minchiu, 46, 47,
Montgomery, 15,
Morgan, 97', 100,
524, 569, 570,
579, 580, 581,
605, 647
Morin, 179, 289
Morse, 407, 408,
415, 416, 417
Mortensen, 464,
566, 567, 576,
Mailer, 196, 204,
445, 447, 454,
501, 502, 508,
567

61, 95,
284, 290,
539, 566,
649

52, 354
16, 31
242, 289,
574, 575,
584, 591,

412, 414,

490, 540,
581

289, 439,
455, 489,
533, 566,

Newstead, 626, 648

Patten, 233, 289, 291, 299,
300, 301, 302, 303, 371

Perrier, 544, 555, 558, 567

Pizon, 637, 642, 648

Poyarkoff, 267, 268, 269,
270, 290

Pratt, 82, 101

Prouho, 386, 387, 388, 392,
394, 406

Purcell, 231, 289

Rees, van, 278, 290
Reichenbach, 178, 179, 180,

181, 182, 183, 184, 189,

281, 289

Rittenhouse, 61, 101
Ritter, 570, 581, 582, 637,

647, 648
Robert, 320, 371
Romer, 396, 398, 406
Roux, 524, 658
Russo, 498, 566

Salensky, 122, 123, 127, 635,

648

Sars, 214, 289
Schaxel, 3, 31, 631, 648
Schimkewitsch, 241, 289
Schneider, 387, 406
Schulze, 37, 52
Sedgwick, 20, 21, 29, 31,

169, 170, 171, 174, 176,

189, 204, 257, 288, 650,

663
Seeliger, 386, 396, 398, 401,

405, 406, 523, 544, 545,

550, 555, 567
Selenka, 529, 530, 531, 533,

534, 541, 567
Selys-Longehamps, de, 381,

382, 385, 628, 648

Semon, 529, 530, 533, 536,

538, 567
Sharpe, 19, 31
Shearer, 11, 31, 154, 165,

168, 381, 382, 385, 523,

567

Sheldon, 226, 288
Shipley, 411, 417
Sigerfoos, 348, 371
Spemann, 660, 663
Spengel, 569, 584, 647
Staff, 157, 158, 168
Stafford, 348, 371, 607
Starling, 652

Sukatschoff, 160, 162, 168
Surface, 103, 106, 107, 108,

112, 116, 117, 129

Taube, 192, 289
Theel, 522, 566
Thompson, 651, 663
Tonniges, 310, 311, 312,

371

Tower, 271, 277, 290
Treadwell, 129, 168

Ubich, von, 504, 520, 566

Verson, 279, 290
Vialleton, 354, 371

Walcott, 657, 663
Weismann, 12,13, 15, 16, 31
Welldon, 658
Wheeler, 245, 246, 247, 261,

290

Whitman, 129, 160, 168
Wierzejski, 291, 320, 321,

323, 338, 340, 371
Wi.jhe, van, 606, 647
Willey, 596, 603, 604, 619,

622, 625, 626, 647, 648
Wilson, C. B., 119, 127
Wilson, E. B., 13, 15, 17,
31, 81, 86, 87, 88, 101,
119, 124, 127, 129, 130,
133, 155, 156, 168, 291,
292, 296, 306, 307, 325,
326, 329, 332, 333, 371
Wilson, H., 206, 289
Woltereck, 106, 128, 140,
144, 147, 153, 164, 165,
168

Yatsu, 119, 124, 126, 127

Zeleny, 119, 124, 127
Zelinka, 418, 419, 426, 427
Ziegler, 89, 91, 101, 349,

371

Zqja, 96, 101
Zur Strassen, 439, 443, 445,

448, 449, 450, 451, 454,

455, 529

INDEX

Abdomen of original Crustacea, function of,

212
Abdominal appendages of Astacus, 188 ;

of caterpillar larva, 286 ; of embryo of

Blatta, 262 ; of embryo of Donacia, 252 ;

in embryos of Hymenoptera, 266 ; in

embryos of Lepidoptera, 266 ; of embryo

of Limulus, 237 ; of Machilis, 265 ; of

embryo of Melolontha, 266 ; of embryo of

scorpion, 240
Abdominal region of embryo of Donacia,

251

Aboral coelom of Antedon rosacea, 552
Aboral disc of fixed larva of Asterias,

470
Aboral nervous system of Antedon rosacea,

formation of, 557
Aboral sinus, formation of, in Anrphiura

squamata, 501 ; in Aster in a gibbosa, 481 ;

in Echinus esculentus, 520
Aboral spike of larva of Echinocardium

cordatum, 522
Aboral tentacles of Tubular ia, formation

of, 55

Acanthobdellidae, 128
Acarina, 221 ; development of, 242
Accessory adductor muscle of Cyphonautes

larva, 393
Accessory retractor muscles of larva of

P/iascolosoma, 376

Achromatic spindle, appearance of, 6
Achtheres ambloplitis, 649, 651 ; development

of, 205-208
Acmaca, 300, 317, 320 ; metamorphosis of

larva of, 306
Acoelida, 102, 103
Acron segment of Donacia, 252 ; of Insecta,

282

Acrosome of spermatozoon, definition of, 7
Actinia bermudensis, development of, 84
Actinia cquinn, development of, 83, 84
A ctinosphaerium, 170
Actinotrocha larva of Phoroitis, structure of,

381, 382
Actinozoa, 53, 166, 661 ; development of,

76-87 ; development compared with that

of Ctenophora, 96
Actimila larva of Tubularia, 56
Adamsia palliata, 85

Adambulaeral plates of Amphiura squamata,

formation of, 499
Adductor muscle of adult Unio, formation

of, 353

Adductor muscle of Cyphonautes larva, 393
Ad oral ciliated band of larva of Asterias,

formation of, 462 ; function of, 463 ; of

larva of Ophiotfvrix fragilis, 487 ; of larva

of Synapta digitata, 532
Adradial cushion of larva of A iirelia, 92
Affinities of Amphiorus with Enteropneusta,

605-608

Affinities of the Enteropneusta, 584-586
Ayariria, larva of, 84
Age.le.na, development of, 221-236
A/jflcna Itibi/riiiflncii, 221
Alcyonaria, 53, 76, 83 ; development of, 86-

88 ; digestion of, 81, 82 ; formation of

skeleton of, 88

Alcyonidium, development of bud of, 398
Alcyonidium albidum, 394
Alci/oit i<!in i/t polyoum, larva of, 395
Alcyonium, 86
Alecithal egg of Amphio.rii.s lanc<',ilnhix,

587

Alima larva of Stomatopoda, 218
Alimentary canal of Bugula, formation of, in

bud, 397

Alloiocoelida, 102, 103
Alternation of generations in Hydrozoa, (i I ;

in Polyzoa ectoprocta, 396 ; in Spongilla

lacvstris, 50

Alveoli of Echinus esculentus, 520
Ambloplitis rupeslris, 206
Ambulacral plates of Asterina gibbosa, origin

of, 478

Ambulatory legs of Attorns, 188
Amnion, formation of, in rinbryo of /><III,I<-I'H,

249 ; in Doryphora, 261 ; in larva of

Erliiniis I'.irii/rii/its, 514; in embryo of

Lepisina, 265; in embryo of M«,-liilix,

265 ; embryo of scor])ion, 240
Amniotic fold in larva of J'n/i/,/in-i/ii/s Im-teus,

151
Amniotic invaginalinii, formation of, in larva

df Kflilinis esculentus, 512
Amniotic invaginations in Pilidium larva of

Nemertinea, 122
Amoeba, 27

667

668

INVERTEBEATA

Amphibia, 569

Amphiblastula larva, of Espcria, 44 ; of

Grantia, 39 ; of Leucosolcnia, 47 ; of

Oscarella, 43

Amphidisc of bud of Ephydatia, 49
Amphioxus, 569, 582, 583, 605, 606, 607,

608, 618, 619, 625, 627, 640, 654 ; larva

of, 28
Amphioxus lanceofatus, development of,

586-604

Amphipoda, 177, 193, 219
Amphitrite, 153
Amphiura squamata, 484, 503 ; post-larval

development of, 498-501
Ampulla of Ophiothrix frar/ilis, formation of,

491
Ampullae of chambered organ of Antedon

rosacea, formation of, 552
Anal cerci of Blatta, formation of, 262
Anal cone of larvaof Pedicel-Una cchinata, 400
Anal field of larva of Asterias, 464
Anal ganglia of Agelena, formation of,

230
Anal loop of ciliated band of larva of Synapta

digitata, 532 ; of ciliated band of New

England Tornaria, 576
Anal papilla, formation of, in Loligo, 358
Anal vesicle of larva of Eupomatus, 154
Anamorpha, 284
Anaspida, 177

Ancestral form of Arachnida, 244
Ancestral history of Porifera, 51
Ancestral significance of Pilidium larva, 127
Anisopleura, 291
Anisopoda, 177, 219
Annelida, 105, 108, 169, 171, 172, 204,

205, 312, 313, 321, 372, 400, 401, 405,

406, 408, 414, 415, 416, 427, 433, 435,

455, 529, 561, 562, 569, 571, 574, 655,

659, 661, 662 ; affinities of, 163-168 ;

affinities with Mollusca, 368 ; development

of, 128-168 ; development of unfertilized

eggs, 17 ; eggs of, 11
Annelidan cross, definition of, 133 ; formation

of, in segmenting eggs of Gastropoda, 322 ;

in embryo of Patella, 294 ; in embryo

of Phascolosoma, 374 ; in embryo of

PoJygordius, 133, 134
Anodon, 352

Anomura, 177, 208, 213, 216
Antedon, 22, 565

Antedon rosacea, development of, 540-558
Antenna, formation of, in Astacus, 184 ; in

Callidina russeola, 426 ; in Pcripatus

capensis, 171 ; in Trilobite, 238
Anteunary sac in larva of Cyclops, 197
Antennary segment of Donacia, 252
Antennulary ganglion of A stacus, 184
Auteunules of Astacus, formation of, 184
Anterior adductor muscle of Dreissensia,

formation of, 342
Anterior amniotic fold in embryo of Donacia,

250 ; absent in embryos of Odonata, 266 ;

present in embryos of Orthoptera, 266

Anterior aorta of Donacia, formation of, 257

Anterior chamber of eye in Loligo, formation
of, 363

Anterior ciliated epaulettes of larva of
Echinus esculentus, formation of, 511

Anterior coelom, formation of, in embryo
of Antedon rosacea, 547 ; in larva of
Asterias, 468 ; in Balanoglossus davigerus,
571 ; in young Antarctic Cucumaria,
542 ; in larva of Ophiothrix fragilis, 490;
in larva of Synapta digitata, 533

Anterior endoderniic thickening, formation
of, in embryo of Donacia, 253

Anterior funnel fold in embryo of Loligo,
357

Anterior mantle - groove of Terebratulina
septentrionalis, 410

Anterior mesenchyme cell in embryo of
Cynthia partita, 615

Anterior mesoderm of Ascaris megalocephala,
formation of, 444

Anterior vacuolated crest of larva of Ophio-
thrix frag His, 486

Antero-dorsal arm of ciliated band of larva
of Asterias, 464 ; of larva of Echinocar-
dinm cordatum, 522 ; of larva of Synapta
digitata, 533 ; of New England Tornaria,
576

Antero-lateral arm of ciliated band of larva of
Ophiothrix fragilis, 489

Antero-lateral rods of larva of Ophiotliri.i-
fragilis, 487

Anura, 657

Anus, disappearance of, in larva of Ophio-
thrix fragilis, 495 ; formation of, in
Amphioxus lanceolatus, 592 ; in Astacus,
183, 185 ; in adult Asterias, 471 ; in larva
of Asterias, 461 ; in Balanoglossus cluri-
gerus, 571 ; in Ciona intestinalis, 625 ;
in Crania, 414; in adult Echinus escu-
lentus, 520 ; in Lingula, 414 ; in Loligo,
358 ; in larva of Membranipora, 390 ; in
Patella, 299 ; in Peripatus capensis, 171 ;
in larva of Phascolosoma, 377; in Poly-
gordius, 144

Apical cells, formation of, in embryo of
Patella, 294 ; in embryo of Phascolosoma,
374 ; in Planocera, 110

Apical invagination of larva of Phylactolae-
niata, 395

Apical organ of larva of Cyclostomata, 395 ;
of Cyphonautes larva, nature of, 392 ; of
embryo of Membranipora, formation of,
388

Apical plate, formation of, in embryo of
Antedon rosacea, 547; in larvaof Balano-
glossus davigerus, 572 ; in Colliding rus-
seola, 423 ; in embryo of Dreissensia,
337 ; in larva of Echinus, 516 ; in larva of
Echiuroidea, 163; in embryo of Patella,
296 ; in embryo of Pedicel-Una, 399 ; in
larva of Terebratulina septentrionalis, 411

Apical sense-organ, formation of, in Bero'e,
94 ; in Cerebratulus lacteus, 120

INDEX

669

Apical string in larva of Balanoglossus
clavigerus, formation of, 573

A/ih/sia, 324

Appendages of branchial hearts of Loli/jo,
development of, 364

Appendages, formation of, in embryo of
Agelena, 225 ; in embryo of Asdici/*,
183; in embryo of Donacia, 252; in
embryo of Peripatus capensis, 171

Appendages of Trilobita, 239

Appendicular sinus in Peripatus capensis, 1 74

Aptera, 245, 263, 265

Apus, 200 ; ancestral, origin of, 212 ; com-
pared to Zoaea, 211

Araclinactis, larva of Cereanthidae, 85

Arachnida, 169, 177, 204, 205, 251, 254,
285, 662 ; development of, 221-244

Araneina, 221

Archaeocytes of Plakina, 44

Archeuteron, formation of, in embryo of
Antedon rosacea, 545 ; in larva of Asterias,
461 ; in larva of Asterina gibbosa, 472 ; in
embryo of D'istaplia, 632 ; in larva of
Echinus esculentus, 507 ; iu larva of JIolo-
thuria tubulosa, 541 ; iu Peripatus capensis,
171; in embryo of Pyrosoma, 633 ; in larva
of Synapta digitata, 531 ; in Terebratu-
lina septentrionalis, 409 ; segmentation
of, iu embryo of Antedon rosacea, 546

Archiannelida, development of, 128-153

Archicerebrum of Scolopendra, 283

Archiuephrklium ofla.rva.of Eupomatus, 154;
formation of, in larva of Polygordius, 138,
140, 144; of Polygordius lacteus, 152

Arenicola, 129, 153

Arenicolidae, 157, 168

Argwpe, 416, 455

A njiope neapolitana, 407

Aristotle's lantern, formation of, in Echinus
esculentus, 515

Anns, formation of, in Antedon rosacea,
556; in Asterias, 469, 470; in Asterlna
gibbosa, 474 ; in Ophiothrix fragilis, 492 ;
in Solaster, 482 ; in Terebratulind sep-
tentrionalis, 413

Arrow-worms, 428

Artliropoda, 455, 655, 656, 661, 662 ; cuticle
of, 19 ; development of, 169-290 ; fossil
representatives of, 20

Arthrostraca, 177

Artificial parthenogenesis of eggs of Echi-
noidea, 524

A scar in, 659

Ascaris megalocephala, development of, 437-
447

Ascidiacea, 568, 608

Ascidiacea compositae, 568, 609, 637, 646

Ascidiacea luciae, 568, 609, 632, 637

Ascidiacea simplices, 568, 609, 637, 646

Ascidians, 98 ; eggs of, 11

Ascidian tadpole, 65

Ascidiozooids of Pyrosoma, 640

Asconidea, 37 ; development of, 46, 47

Asexual germ, definition of, 2

Asexual reproduction in Urochorda, 637-646

Aspidobranchiata, 291, 301

Asplanchna Herricki, 418

Asplanchnidea, 418

Astacidae, 213

Astacus, 191, 194, 195, 197, 198, 223,

230, 235, 236, 243, 281
Astacus Jluviatilis, development of, 178-189
Aster, formation of, from middle piece of

spermatozoon, 9
Asterias, 474, 475, 476, 477, 478, 483, 484,

485, 487, 495, 503, 506, 507, 514, 525,

569 ; development of, 460-472
Asterias glacialis, 464, 466, 472, 492, 505
Asterias pallida, 457

Asterias rubens, 457, 461, 464, 466, 472, 529
Asterias vulgar is, 401, 457, 464, 465, 472
Asterina gibbosa, 457, 482, 495, 536, 569,

656 ; development of, 473-481
Asteroidea, 287, 456, 494, 495, 496, 497,

498, 500, 501, 502, 503, 514, 515, 518,

520, 521, 522, 523, 530, 531, 533, 535,

538, 541, 543, 560, 563, 564, 565, 569,

585 ; development of, 457-484
Astropecten, 457
Astropectiuidae, 472

Asymmetry of post-larval Pagurid, 65, 216
Atrial cavity, formation of, in Amphio.i-u*

lanceolatus, 599 ; in Molgula anipullmdes,

632 ; in Aseidiozooid of Pyrosoma, 640 ;

in Blastozooid of Urochorda, 638
Atrial folds, formation of, in larva of ^-1 mp/i /'-

oxus lanceolatus, 599
Atrial imagination, formation of, in larva

of simple Ascidian, 620 ; in larva of

Itoliolum, 637 ; in embryo of Pyrosoma

634

Atrial tube of embryo of Pyrosoma, forma-
tion of, 634
Atrium, formation of, in bud of Buytihi,

397 ; in embryo of Membranipora, 389 ;

in embryo of Pedicellina echinata, 400 ;

in larva of Pedicellina echinata, 400 ;

in Physa (outer stomodaeum), 323 ; iu

larva of Synapta, digitata, 536
Atrochal larva, definition of, 153
Auditory organ of Astacus, 189
Aurelia, development of, 67-73
Auricle of heart, formation of, in Cyclas, 350 ;

in Luli;/o, 362
Auricularia larva, 561, 574, 585 ; structure

of, 533
Axial organ, formation of, va. Antedon rosacea,

552 ; in Asterina yibbosa, 480
Axial sinus, formation of, in Asterina gibbosa,

475 ; in Echinus esculentus, 510
Axolotl, 656

Azygous tentacles of Antedon rosacea, forma-
tion of, 556
Azygous tube-feet, formation of, in Asli-rinn

gibbosa,476 ; in /,'<•// ////>,v >-.•«• H I ,-n his, 518 ;

in Op// intli ri.r /'rinjilis, 492

Balanoglossida, 568, 569, 575, 585, 589, 6tJ2

670

INVERTEBRATA

Balanoglossus, 1, 381, 467, 584, 587, 605

Balanoglossus davigerus, 575 ; development
of, 570-574

Ball eggs of A scar is nieffaloeephala, 453

Barrel-shaped larva of Synapta digitata, 538

Basal cells in Molhiscan cross iu eggs of
Gastropoda, divisions of, 322 ; in Mollus-
cau cross in embryo of Patella, 294

Basal plates, formation of, in Arnphnna
squamata, 499 ; in Caryophyllia, cyathus,
87

Basal ring of plates in larva of Antedon
rosacea, formation of, 547

Bathycrinus, 559, 560

Bdelioida, 418

Bell rudiment of Medusa of Tubularia, 58

BerOe, development of, 89-95 ; experiments
on eggs of, 96, 97, 98

Beroe forskalii, 89

Bertie ovata, 89

Beroidea, 53

Biogenetic law, 20, 649

Bipiuuaria larva, 472, 474, 483, 487, 490, 491,
492, 529, 532, 533, 542, 543, 574, 585 ;
of Asterias, 464 ; of Astropectiuidae, 472

Birds, fertilization of eggs of, 12

Bivalens, race of A scar is megalocephala,
439

Bivalve shell of Cyphonautes larva, 392

Bladder of Callidina russeola, formation of,
426

Blastocoele in Actinotrocha larva, 382 ; in
egg of Agelena, 223 ; formation of, in
embryo of Antedon rosacea, 545 ; in larva
of Asterias, 461 ; in embryo of Cynthia
partita, 614 ; in embryo of Dreissensia,
333 ; iu larva of Echinus esculentus,
506 ; in Grantia, 38 ; in embryo of Mem-
branipora, 387 ; in Patella, 295 ; in Poly-
gnrdins, 140 ; equivalent to haemocoele,
1 72 ; equivalent to primary body-cavity,
165

Blastocones in egg*uof Sepia, 355

Blastoderm, formation of, in Astacus, 180 ;
in Scolopendra, 281 ; in Sepia, 355

Blastoidea, 456

Blastomere, definition of, 27

Blastomeres of egg of Cynthia parti/n.
development of when isolated, 630 ; of
egg of Sepia, 354

Blastoporal pit of embryo of Blatta, 261

Blastopore, closure of, in- embryo of Amplii-
oxus lanceolatns, 591 ; in embryo of
Antedon rosacea, 545 ; iu embryo of
Ascaris megalocephala, 445, 446 ; in em-
bryo of Astacus, 182 ; in Balanoglossus
davigerus, 571 ; in embryo of Cynthia
partita, 619 ; in embryo of Dreisxensitt,
336; iu embryo of Euphausia, 192; of
embryo of Membranipora, 388 ; in embryo
of Patella, 298 ; in embryo of Pedicel! inn,
399 ; in embryo of Pyrosoma, 634 ; of
Sagitta bipunctata, 431 ; of Terebratulina
septentrional is, 409, 410

Divided into month and primitive aims
in embryo of Polygordius, 139

Persistence of, in larva of Asterias, 461 ;
in embryo of Aurelia, 68 ; as mouth
and amis in embryo of Peri/iatn* citpeiisis,
171

Represented by primitive streak and
primitive cumulus in Arachnida, in an
embryo, 241

Blastostyle of Clava, 62

Blastozooid in Diplosomidae, development of,
642-644 ; of Salpa, 640 ; in Urochorda,
definition of, 638

Blastozooids (buds) of Dolioluni, 640, 641

Blastula of Amphioxus lanceolatus, 589 ; of
Antedon rosacea, 545 ; of Ascaris iiicgalo-
cephala, 443; of Astacus, ISO; of Asteri</x,
460 ; of Aurelia, 68 ; of Balanoglossus
davigerus, 570, 571 ; of Callidina russeola,
422; of Cerebratulus lacteus, 119; of Clath-
rina, 47 ; of Cucti/naria planci, 541 ; of
Cynthiapartita, 614; of Echinus esculentus,

507 ; of Euphausia, 192 ; of Grantia, 38 ;
of Holothui'ia tubulosa, 541 ; of Leuco-
solema, 47 ; of Macrobiotus, 243 ; of
Ophiothrix frag His, 486, 487; of Ophiura
brevispina, 501 ; of Oscarella, 43 ; of
Pallene, 243 ; of Patella, 295 ; of Pedi-
cellini, 398 ; of Plakina, 44 ; of Polygor-
dius, 132, 139 ; of Polyphemus, 193 ; of
Sagitta bipunctata, 429 ; of Synapta digi-
tata, 530 ; of Terebratulina septentrionalis,
408, 409 ; of Tubularia, 54 ; of Urticina
crassicornis, 77 ; formed from egg of free
medusa, 59 ; interpretation of, 660

Blatta, 288 ; embryonic development of,
261, 262

Blood-spaces of Loligo, formation of, 361,
362

Blood-system of Echinus esculentus, forma-
tion of, 518

Blood-vessels of Polygordius appenSiculatus,
formation of, 152

Body-rods of larva of Echinus esculentus,

508 ; of larva of Ophiothrix fragilis, 487
JSn/iiia, experiments on the eggs of, 98
Boinbyx mori, metamorphosis of, 279,

280

Borax-carmine, use of, 35
Botryllidae, 642
Botryllus, 638, 644 ; development of buds

of, 641, 642

Brachiolar anus of larva of Asterias, 467
Brachiolaria larva, 565 ; of Asterias, 467-

469
Brachiopoda, 435, 585, 661 ; development

of, 407-417

Brachyura, 177, 208, 213, 215
Brain, formation of, of Cal/idina russeola,

424 ; of Sagitta bipunctata, 432
Brain- vesicles, formation of, in Antedon

rosacea, 557 ; in larva of Cynthiapartita,

619
Branchial cavity of Astacus, 188

INDEX

671

Branchial heart of Lulign, formation of,

362, 364
Branchiopoda, 177, 194 ; larval history of,

200
Ijnnicliipiix, 194, 196,243; ancestral origin

of, 212

Brephic stage, development of, 1 9, 22
Buccal cavity, formation of, in Amphioxus

lunceolatus, 604 ; in Peripatus capensis,

175

Buccal cirri of Amphioxus lanceolatus, forma-
tion of, 606
Buccal tentacles, formation of, in Cucumaria

planci, 542 ; in Synaptu diyifata, 533
BIT!, definition of, 2 ; development of, in

Alcyonidinin, 398 ; in Pcdiccllitia edihtata,

403; in Spongilla, 47
Building in Polyzoa Ectoprocta, 396-398 ;

in Urochorda, 637-646
Buc/ula, corona of larva of, 395 ; development

of buds of, 396-398
Buprestidae, 272, 277, 278
Butyric acid, use of, to produce membrane,

17, 524
Byssus gland of Dreissensia, formation of, 342

Calanus, 206
Calcarea, 57

Calcareous plates of young Cucuimiria, 542
Calcareous ring of Syiiapta digitata, forma-
tion of, 539
Calcareous skeleton of adult Aster ina gibbosa,

formation of, 477, 478

Calcareous sponges, development of, in lime-
free water, 51

Callianira, development of, 95
Callidinii russeola, development of, 418, 426
Calyptoblastea, 53 ; definition of, 62
Calyptopis, larva of Euphausiadacea, 209
Calyx of Antedon rosacea, formation of,

551

('apitella, 153, 167
Capitellifornia, 128, 153
Capsules containing eggs of Alloiocoelida,
Rhabdoeoelida, Triclada, Cestoda and
Trematoda, 102, 103 ; containing eggs of
Prosobranchiata, Opisthobranchiata, and
Pulmonata, 320

Carapace of Astacus, 185 ; of pupa of

Cirripedia, 202 ; of larvae of Euphausia

and Penaens, 203 ; of Nauplius, larva of

Ostracoda, 203

Cardioblasts, formation of, in Clepsine, 163 ;

in Ihmuciti, 256
Gardium, 348

(.'rti-idea, 177, 208, 213, 215
( 'ariua of Cirripedia, formation of, 202
Cartilage of Cephalopoda, formation of, 365
Ccvryophylliacyathus,Aeve\opioen.tofBkeleion

of, 87
Cataclysmic metamorphosis, definition of,

127

Caterpillar larva of Lepidoptera and Hyineii-
optera, 266

Cathamnial plate of A urdin, development of,
73

Caudal fork of A stums, 187 ; of Cydiijix,
formation of, 199

Caudal lobe in the embryo of Agelena, 224

Caudal spine of Nauplius larva of Cirripedia,
201

Cell-lineage, definition of, 104 ; of eggs of
Hirudinea, 160 ; of eggs of Ischnochiton,
320 ; of eggs of Patella, 292-295 ; of eggs
of Phascolosoma, 373-375 ; of eggs of
Physa, 321 ; of eggs of Planocera, 104-
109; of eggs of Polygordius, 131-144

Celloidin, use of, in embedding, 34, 35

Cement organ of embryo of Pedicettina, 399

Centipedes, 281

Central coelom of Cribrella, development of,
481

Central eyes, formation of, in Limulus, 237 ;
in Agelena, 232-234

Centriole of male cell, 7

Centre -dorsal ossicle of Antedon rosacea,
formation of, 558

Centrolecithal, definition of, 27 ; segmenta-
tion of eggs of Crustacea, Arachnida, and
Myriapoda, 177

Centrolecithal egg of Urticina crassicornis,
177

Centroplasm of egg of Agelena, 222

Ceutrosome, division of, 6 ; formed from
middle-piece of spermatozoon, 9

Cephalic hood of Say Ma bipunctata, 432

Cephalic lobes in embryo of Agelena, 224
in embryo of Astacus, 180, 189 ; in
embryo of Scorpion, 240

Cephalic slits of Neinertinea, formation of,
in Pilidium larva, 123

Cephalochorda, 568, 584, 605, 662 ; develop-
ment of, 586-604

Cephalodiscida, 568, 569, 585, 606, 662

Cephalodiscus, 381, 383

Cephalopoda, 178, 291, 369, 370, 632 ; de-
velopment of, 353-368

Cerambycidae, 272, 277

Cereanthidae, 53, 86 ; larva of, 85

Cerebral ganglion, formation of, inDentaUum,
329 ; in Dreissensia, 341 ; in Loliyo, 358 ;
in Palndina, 315 ; in Patella, 301, 302;
in embryo of Pedicdlina, 400; in larva of
Phascolosoma, 376 ; in Planocera, 11Q ; in
Planorbis, 322

Cerebral grooves, -closure of, in embryo of
Agdi'iia, 232 ; formation of, in embryo of
Aydena, 225; in embryo of Ax/nnix,
184 ; in embryo of Peripatus capensis,
175

Cerebral pit, formation of, in larva of />;v/\-
sensia, 341 ; in embryo of J'fdicif/i/ni,
400

Cerebratul-uslacteus, development of, 118-126

( Vstidea, 53

Cestoda, 102, 103

Chaeta sacs of larva of Terebratulina
septentrional is, 411, 413

INVERTEBKATA

Chaetae of larva of Terebratulina septentrion-
al is, 411, 413

Chaetognatha, 454, 455 ; development of,
428-436

Chaetopocla, 128

Chambered organ, formatiou of, in Antedon
rosacea, 549

Clieilostomata, 386, 394

Cheliceral ganglia, fate of, in Agelena, 232

Cheraphilus, Mysis larva of, 215

Chilaria of Liinulus, formation of, 237

Chilopoda, 280, 281, 284. 285

Chin in larva of simple Ascidian, 622

Chitin, nature of, possibly allied to uric acid,
176

Chiton, 320, 322

Chiton pulii, 320

Chlomxtunni, 523

Chondrostei, 569

Chorda-neural cells in embryo of Cynthia
partita, origin of, 614

Chordata, 568. (See Vertebrata.)

Chorion of egg of Cynthia partita, 610 ;
definition of, 3

Chromatin, emitted into cytoplasm of egg, 3

Chromosome, accessory, 14

Chromosomes, definition of, 2 ; division and
fusion of, 4 ; bivalent, 12

Chrysomelidae, 267, 277, 278, 279

Ciliary body of Cephalopod eye, formation of,
367

Ciliated filter in gut of larva of Polygordius
appendiculatus, 149

Ciliated groove in Annelid larvae, 174 ; in
larva of Capitella, 156, 167 ; in larva of
Echiurus, 167 ; in larvae of Echiuroidea,
163 ; in larva of Patella, 309 ; in larvae
of Solenogastres, 325

Ciliated lobes, formation of, in larva of
YungM, 112, 113

Ciliated pits, formation of, in Polygordius
appendiculatus, 148

Ciliated tentacles, formation of, in Phascolo-
soum, 379

Ciugulum, formation of, in Callidina russeola,
425

dona, 631, 645

dona intestiiialis, 609, 619

Circular muscles, formation of, in Nephelis,
162 ; in Criodrilus lacuum, 158

Cirripedia, 177, 185, 622, 655, 656 ; ances-
tral origin of, 213 ; development of
(formatiou of layers), 195 ; larval history
of, 201, 202 ; pupa of, 28, 202

Cistella neapolitana, 407

Cladocera, 177, 662; ancestral, origin of,
212 ; larval history of, 200

Classification of Annelida, 128 ; of Arach-
nida, 221 ; of Arthropoda, 169 ; of
Brachiopoda, 407 ; of Coeleuterata, 53 ;
of Crustacea, 177 ; of Echinodermata
456 ; of Insecta, 245 ; of Mollusca, 291
of Nemertinea, 118 ; of Platyhelmiuthes
102 ; of Podaxonia, 372 ; of Polyzoa, 386

of Porifera, 37 ; of Protochordata, 568 ; of
Rotifera, 418

Clathrina, 46

Clava, umbrella cavity of, 63 ; development
of genital cells of, 62

Clavelina, 619, 632, 638, 644, 646

Cleavage, see Segmentation of egg

L'lepsine, 161

Cloaca of Ascaris megalocephala, 438 ; forma-
tion of, in embryo of Pyrosoma, 634

Closed dwarf larvae of Patella, 307

Club-shaped gland, formation of, in larva of
Aiirphio.cus lanceolatus, 596

Clytia, medusa of, 59 : experiments on the
eggs of, 96, 97

Coelenterata, 116, 161, 166, 457, 561, 661;
development of, 53-101

Coelenterou, formation of, in Tubt/laria, 55;
in Urticina crassicornis, 79

Coelom, ancestral origin of, 165

Division of, in embryo of Dreissensia,
343 ; in larva of Synapta digitata, 533

Formation of, in Actinotrocha larva,
382 ; in embryo of Amphioxus lanceolatus,
592 ; in embryo of Angelena, 225, 226 ;
in embryo of Argiope, 416 ; in embryo
of Astacus, 187, 189 ; in larva of Asterias,
461 ; in larva of Asterina gibbosa, 472 ;
in embryo of Blatta, 261 ; in bud of
Bugula, 398 ; in embryo of Callidina
russeola, 427 ; in embryo of Cribrella,
481 ; in embryo of Cucumaria planci,
542 ; in larva of Dolichoglossus komi-
levskii, 582 ; in larva of Dolichoglossus
pusillus, 583 ; in embryo of Donacia, 253 ;
in embryo of Dreissensia, 337 ; in larva
of Holothwria tubidosa, 541 ; in embryo of
Loligo, 361, 362 ; in embryo of JUacro-
biotus, 243 ; in embryo of Nephelis, 163 ;
in larva of Ophiothrix fragilis, 487; in
embryo of Ophiura brevispina, 501 ; in
embryo of Paludina, 311 ; in embryo
of Peripatus capensis, 171 ; in larva of
Pliascolosoma, 377 ; in larva of Polygor-
dius, 138 ; in embryo of Sag Ma bipunc-
tata, 430 ; in embryo of Scolopendra,
283 ; in larva of Synapta digitata, 531 ;
in embryo of Terebratulina septentrionalis,
409; modification of, 411; in larva of
Unio, 352

Coelom-formiug substance in the eggs of
Asterias, 483

Coelomic ganglia, formation of, in Op/t /«////•/>
fragilis, 498

Coelomic grooves, formation of, in embryo of
A mphioxus lanceolatus, 592

Coelomic sacs, formation of, in larva of
Asterias, 461 ; in larva of Ophiothrix
fragilis, 487 ; segmentation of, in Sagitta
bipunctata, 431

Coelomiduct, nature of larval kidney of
Gastropoda, 323

Coelomiducts of Brachiopoda, 407

Coleoptera, 245, 261, 262, 266, 277

INDEX

Gi— ••>
/o

Collar of New England Tornaria, formatioii

of, 577
Collar-cavities, formation of, ill Actinotrocha

larva of I'liorouis, 381
Collar-ooeloin, formation of, in New England

Tornaria, 575
Collar-pores, formation of, in Actinotroeha

larva of I'/wriihin, 381 ; in Nassau Tornaria,

580
Collar-skeleton, formation of, in New England

Tornaria, 579
Collembola, '245
Columella, formation of, in L'<(i'(/<~ij.>hylUa

c//iif/iii.-i, 88
Columnal plates, formation of, in larva of

Antci/ini ri'sucea, 548, 550
Comb of cilia in Beroe, 94 ; in embryo of

J'ufcllii, 296

Comb of scorpion, formation of. 240, 241
Comparative embryology, definition of, 29
Comparison of Bipinnaria and Ophiopluteus

larvae, 491, 492 ; of development of

nrli '<ntlir is and J.-Vir/cs, 503, 504 ; of

larvae of Ojjliiof/iri.i- fruyilis and of

Echinus esculeiitns, 511
Compound eye in Inseeta, 286 ; in Trilobita,

Crustacea, Arachnida, 286 ; development

of, uiAxtactt-s, 184 ; in Dyatii-nx mm-ijinaUs,

271-277

Conjugation, definition of, 2
Copepoda, 177, 185, 649, 651, 655, 662 ;

ancestral origin of, 213 ; development of

(formation of layers), 195 ; larval history

of, 196-200, 206-208

Copepodid larva of Adheres ambloplitis, com-
pared to normal Copepod, 206, 208
Copulation path of nucleus in egg of (Jynfliiii

purlitu, 611
Copulatory spicules of A scar is megalocephala,

438

C'oral, formation of, 87, 88
Cordylophora, development of gonophore of,

62
Corneal fold, formation of in eye of Zo//</«,

363, 367

Corneal lens of eye of Astacus, 189
Corona in larva of llni/n/a, 395 ; in larva of

Cyclostomata, 395 ; in larva of Lepr«Ii<i,

395 ; in larva of J//'//^/v /<//>'</•<', 390 ; in

embryo of Pedicellina, 400 ; in larva of

Pliylactolaemata, 395
Corpus epitheliale, formation of, in Cephalo-

jiod eye, 367

Corrosive sublimate, use of, 33
<.'nt//Jni-]i!~n, development of, 73
Couples of mesenteries of Urticina croxxi-

<•"/•// /X 80
Coxal gland, formation of, of Ai/eleita, 229-

230 ; in Li in u! as, 236 ; in Scorpion, 2-11
Ci'itiii/uti, larva of, 215
Crania, 414
Crej/iilulH, 291, 323 ; segmentation of egg

of, 321
Crepidula . plana, eggs of, 10, 11

VOL. I

Cribrella, 484, 656 ; development of, 481

(.'rilnr//<i in'iiliitii, 4."i7, 459

Crinoidea, 450, 523, 561, 5C2, 563, 564, 5s5,

622 ; development of, 5 1 1-fiiiU ; sperm of,

used to cross-fertilize eggs of sea-urchins,

17

Criodrilus, 147, 162

('/•jiit/i-i/iix l<t<-itiiiii, development of, 157, 159
Cross-furrow in the egg of I',ii,-Un, 292
Crural glands, formation of, in I'eripaliis

<•<//« nsis, 175
Crustacea, 22, 169, 244, 254, 280, 286 ;

development of, 177-220
Crystalline cone, formation of, in compound

eye of A.xttx'ii.s, 189 ; in compound eye of

Dytiscux, 276
Crystalline sac, formation of, in Dreissc»*i<t,

340
Crystalline style, formation of, in Dreisseiixio,

340
Ctenophora, 53, 115, 116, 117, 126, 127,

148, 164, 166, 167, 296, 309, 416, 529,

561, 562, 659, 661 ; development of, 88-95
Ctenophore stage in the embryo of ]'<it<'II,i,

296

Cteniiji/iiiin, 115
Ctenostomata, 380, 394
Cucumaria, 547

Qucumaria jitum-i, 529, 534, 535 ; develop-
ment of, 541

Cucumaria xa.i.'icvla, 530, 543, 514
C'ulieidae, 278
Cumacea, 177, 219
Cumulus primiiivus in embryo of AV.i/iy/r mini,

282

Cuticle of I'l-i-ipfitux <•« /ifusis, 176
Cyathozooid cmViryo of Pyrosoma, 635, 640
Cyclas, 349; formation of pericardium of,

350
Cyclops, 200, 201, 206; larval history of,

196-200

Cyclopsinidae, larvae of, 200
Cyclostomata (Polyzoa), 386 ; larva of, 395 :

(Fish), 569, 662

Cynthia partita, 631, 632, 645; develop-
ment of, 609-619
Cyphouautes, larva of Membranipora, 101,

405, 406 ; hatching of, 389 ; rearing of,

387

( 'ystoidea, 456
Cytotaxis, causing imagination in Kcliin-

oidea, 527 ; in Polygordius, 139

Decapoda (Crustacea), 177, 1^.203,208,

218. 219, 286

Dehydration, definition of, 32
Delamination in Ceryonidae, 67
Delobranchiata, 221

Demospoiigiae, 37 ; development ol, 13-46
Dendroeoe'la, In2, 103
Dentalium, '•'>!'•'•, 37"' : development nf, 325-

329
Dental pnekets, toiiuation of. in larva of

Ei-tiiiinx , nulentus, 515

2x

674

INVEETEBEATA

Determinate cleavage, 416
Deuterocerebrumof Astacus, 184; of Donacia,

258 ; of Scolopendra, 283
Deuteroplasin, 19 ; definition of, 3
Deutovum of Mites, 242
Development of larva of Dentaliitm, deprived

of first polar lobe, 330 ; deprived of second

polar lobe, 331

Dexiotropic cleavage, definition of, 104
Diakinesis, definition of, 6
Diminution of the chromatin in segmenting

egg of Ascaris megalocephala, 440
Dinophilus, egg of, 11
Dipleurula larva, 561, 564 ; definition of,

560 ; interpretation of, 661
Diplopoda, 280, 281 ; development of, 284
Diplosomidae, 637 ; development of, buds

of, 642-644
Dipnoi, 569
Diptera, 245, 272, 279
Directive mesenteries, definition of, 83
Disc of fixed larva of Asterias, 469
Discocoelis, 107, 109
Distaplia, 634, 638, 640, 641, 644
Dolichoglossus, 575, 584, 605
Dolichoglossus kowalevskii, 569 ; development

of, 582, 583
Dolichoglossus pusillus, 570 ; development

of, 583
Doliolum, 639, 640, 641 ; development of,

636, 637

Donacia, 261, 263, 265, 266, 267, 272
Donacia crassipes, development of, 245-260
Dondersia, 325
Dorsal aorta, formation of, inAgelena, 229 ;

in Amphioxus lanceolatus, 595
Dorsal arch in skeleton of larva of Echinus

esculentus, 509
Dorsal blood-vessel, formation of, in Clepsine,

163 ; in Echinus esculentus, 518
Dorsal cell family in segmenting egg of

Ascaris megalocephala, 440
Dorsal chamber of Urticina crassicornis, 80
Dorsal ciliated epaulettes, formation of, in

larva of Echinus esculentus, 511
Dorsal cord, formation of, in embryo of

Phascolosoma, 376

Dorsal curvature of embryo of Donacia, 259
Dorsal muscle of Cyphonautes larva, 390, 392
Dorsal nerve-cord, formation of, in Dolicho-

gJossus kowalevskii, 583 ; in New England

Tornaria, 578
Dorsal nerve-tube, formation of, in New

England Tornaria, 578
Dorsal organ, formation of, in Amphiura

squamata, 500 ; in Asterina gibbosa, 480 ;

in embryo of Pedicellina, 400 ; in embryo

of Scolopendra, 284
Dorsal retractor muscles, formation of, in

larva of Dreissensia, 341
Dorsal sinus, formation of, in Nephelis, 163
Dorse-central plate, formation of, in Am-
phiura squamata, 499 ; in Asterina gibbosa,

478

Dorso-lateral chamber of Urticina crassi-
cornis, 80

Dorso-lateral spine of Nauplius larva of
Cirripedia, 201

Dorso-ventral muscles of Yungia, 114

Doryphora, 267, 277 ; development of wings
of, 271-273

Doryphora decemlineata, development of,
245, 246, 247 ; embryonic development
of, 261

Doubly fertilized eggs of Ascaris megalo-
cephala, development of, 451-453

Dreissensia, 349, 350

Dreissensia polym&rgha, development of,
332-348

Dytiscidae, 273

Dystiscv.s marginalis, development of eyes of,
273-277

Ear, formation of, in larva of simple
Ascidian, 620

Ecardines, 407, 414

Ecdysis in Astacus, 185

Echinocardium cordatum, 504, 523 ; develop-
ment of, 522

Echinocyamus pusiUus, 504, 522

Echinodermata, 110, 287, 408, 416, 418,
435, 573, 585, 586, 589, 600, 645, 653,
657, 659, 660, 662 ; development of,
456-567 ; development of unfertilized eggs
of, 17 ; eggs of, 3 ; experiments on eggs
of, 30 ; fossil representatives of, 20 ;
larva of, 19

Echinoidea, 287, 456, 461, 464, 482, 484,
530, 531, 538, 541, 542, 543, 544, 560,
562, 564. 565, 570, 571, 653 ; develop-
ment of, 504-529

Echinopluteus, 280, 527, 532, 533, 551, 560,
565, 573 ; definition of, 490 ; description
of, 508, 509

Echinus, 228, 463, 484, 505, 590, 653, 654 ;
entelechy of, 21

Echinus esculentus, 504, 505, 523, 529 ;
development of, 506-522

Echinus microtuberculatus, 504, 505

Echinus miiiaris, 504, 516, 523

Echinus-rudiment of larva of Echinus escu-
lentus, formation of, 513

Echiuroidea, 163, 372

Echiurus, 167

Ectoderm, definition of, 53 ; formation of,
in Cerebratulus hicteus, 119 ; in Jin-nada,
249; in Pcripiititx capcnsis, 170; in
Planocera, 105 ; in Tubularia, 55

Ectodermal origin (supposed) of mid -gut in
Insecta, 262

Ectodermal vesicles in larva of DdUoliuin,
637

Edwardsia stage in development of Urticina
crassicornis, 83

Edwardsiae, 53, 86 ; arrangement of mesen-
teries of, 83

Eggs of Amphioxus lanceolatus, 586, 587 ;
of Amphioxus lanceolatus, deliisceuce of,

INDEX

675

587 ; of Ai/ff-t/ii/i rosacea, 545 ; of Asteri'.is,
development of, in sulphocyanide of potas-
sium, 483 ; of Balanoglossus clavigerus,
570 ; of Ctilliilinti russe< iJ a, 418 ; of
< ',-,Yh,-ittitlns lacteus, constitution of, 126 ;
of < In ci_ •[ i,/i/, 632 ; of Ctenophora, constitu-
tion of, 98; of Cynthia partita, 610 ; of
Dentalium, maturation of, 325 ; of
Distaplia, 632 ; of Dofichogfossus koival-
eeskii, 5S2 ; of Echiuoidea, methods of
obtaining, 505, 506 ; of Hydromedusae,
constitution of, 98 ; ofOphiothrixfragilis,
485 ; of Planocera, 103 ; of PolygonUii*,
129 ; of Tercl'i-tit alii HI septentrionalis, 408

Egg-shell, outer, 3 (see Chorion) ; inner, 3
(see Vitelline membrane)

Elaeoblast, formation of, in embryo of Salpn,
636

Elasmobranehii, 456, 564, 569

Elevator muscles of larva of P0///</«/v>V/'.s
appendiculatus, 148

Embolobranchiata, 221

Embryo, deh'nition of, 19 ; formed from
larva, 26 ; of Am/ili i i< rn S'/tmi/n'ta, 498 ;
ofVertebrata, compared with Coelenterata,
53

Embryology, scope of, 1

Embryonic area, in egg of Blatta, 261 ; in
egg of Diptera, 266 ; in egg of DmHK'!",
249 ; in egg of Doryphom, 261 ; in egg
of Hemiptera, 266 ; in egg of Lepisma,
264 ; in egg of Odoiiata, 266 ; in egg of
Scolopendra, 283, 284

Embryonic phase of development, definition
of, 19 ; interpretation of, 26, 655, 656

Endoderm, definition of, 53 ; formation of, of
Ayelena, 224 ; of Astacus, 180 ; in Cere-
bratnli/s lacteus, 119 ; in Clepsine, 161 ;
in Doiiacia, 248 ; of Euphatisia, 192 ;
in Homarus, 191; in Lepisina, 264 ; in
Liiiiulus, 236 ; in larva of Membra nipon.i,
388 ; in Jfephelis, 161 ; in Palaemon,
192 ; in Pallcnc, 243 ; in Peripatus
capensis, 170 ; in Phascolosoma, 375 ; in
Planocera, 109 ; in Polyphemus, 194 ; in
Sc<'hi)>i:nilra, 282 ; in Scorpion, 240 ; in
Tubi'laria, 55

Eudoderm lamella, erroneous theory of forma-
tion of, 64 ; formation of, in A urelia, 73 ;
in medusa of Podocoryne, 61 ; in medusa
of TuJ •> i>/< T fa, 58

Eudodermal plate of Astacus, 189

Endodermic groove in embryo of
181

Endodermic streaks in embryo of
254

Eudopodite of antenna in Astacus, 186

Eudostyle, formation of, in larva of A mphi-
o.-fus lanceolatits, 596 ; in Cyathozooid
embryo of Pyrosi.itn<t, 635 ; in Pacific
Tornaria, 581, 582 ; in tadpole of simple
Ascidians, 620

Entelechy, 451, 483 ; definition of, 20 ;
theory of, 526
VOL. I

Enteropneusta, 563, 592, 605, 606, 608,

646, 662 ; development of, 569-586
Entouiscidae, 219
Ephemeridae, 655
Ephemeroptera, 245, 272, 287
Ephydiitia, development of gemnuile of, 47-50
Epbyra larva of Anrelia, 72 ; of /'<•/«;//<-<, 74
Epibole, definition of, 92 ; in embryo of

Beroe, 92 ; in embryo of Put, -II, i, 297 ;

in embryo of I'cri^nlns capensis, 171 ;

in embryo of Planocera, 109
Epicardial tubes, formation of, in dona

!ittt'xtini<U,-i, 626
Epigastric coelom in larva of Asterius, 469 ;

in larva of Asterina gibbosa, 475, 480
Epimorpha, 284
Epiueural canals, formation of, in Echinus

esctili-iitH*. 514
K])ineuraly flaps, formation of, in larva of

< >/,!/ i,ttln-i.i- fmyilis, 495
Epineural ridges, formation of, in larva of

Echinus esc ufe lit us, 514
Epineural ring-canal, formation of, inSi/napta

vivipara, 539
Epineural roof, formation of, in C>2)hiothrix

fi'iigilis, 495
Epiueural sinus, formation of, in Donatia,

25 1. 255
Epineural space, formation of, in larva of

Kfliiiiiis esculentus, 514 ; in larva of

Op/ti" i-" '»•< vispina, 502
Epineural veil, formation of, in larva of

Echinus esculentus, 514
Epipodite in Li>iin/its, 237
Epistome of larva of J'cificflliiin, 400
Equating division, definition of, 6
Equatorial plate, definition of, 6
Erichthoidina stage in development of

Stomatopoda, 217
Erichthus stage in development of Stomato--

poda, 218

Eruciforni type of Insect larva, 2.^7
Esperia, 47 ; development of, 44-46
Eucarida, 177
Euphausia, 192
Euphausidacea, 177, 203, 208
Eupomatus, 165, 313 ; development of, 154,

155

Excretory canals, formation of, in Beroe, 95
Excretory organs, formation of, in A HIJI/I ioxus

lanceolatus 600 (see also Kidney and

Nephridiuni) ; in Ascaris megalocephala,

447; in Asffici'd, 188; in CalHtlina rus-

seola, 426 ; in Peripatus capensis, 124
Exopodite of antenna in Astacn.t, IM!
Exopodites of limlis of prosoma in Limulus,

236
Experimental embryology, aim of, 29,

30; of simple Ascidians, i':'>0, 631;

of Asteroidea, 482-484 ; of Calcareous

sponges, 51; of Coeleiiteni -, '.'6-98; of

i:. liinoidea, 522-529 ; of Mollusca, 305-

309, 329-332; <>f Xematoda, 448-454;

of Nemertinea, 124-126

L' X -J

676

INVEETEBEATA

Experiments on the eggs of Ascaris, 448-454 ;
on the eggs of Berde, 96, 97 ; on the eggs
of Bolina, 98 ; on the eggs of Gerebratulus,
124-126 ; on the eggs of dona, 631 ; on
the eggs of Clytia, 96, 97 ; on the eggs of
Cynthia partita, 630 ; on the eggs of
Dentaliuin, 329 - 332 ; on the fertilized
eggs of Echinoidea, 524, 525 ; on the eggs
of Geryonia, 96 ; on the eggs of Laodice,
96 ; on the eggs of Liriope, 96 ; on the
eggs of Mitrocoma, 96 ; on the eggs of
Molgula, 631 ; on the eggs of Patella,
305-309 ; on the eggs of Phallmia, 631

External opening of kidney of Dreissensia,
formation of, 345

External perihaemal ring-canal of Asterina
gibbosa, formation of, 475

External yolk-sac of Loligo, formation of,
360

Eye, formation of, in larva of simple Ascidiau,
620 ; in Balanoglossus clavigerus, 574 ; in
Loligo, 357 ; in Paludina, 315 ; in Patella,
302 ; inPeripatus capensis, 176 ; in larva of
Phascolosoma, 376 ; in larva of Polygordius
appendiculafus, 148 ; mSagitta bipunctata,
433 ; in New England Tornaria, 575

Eyelids, formation of, in Loligo, 363

Eye-spot, formation of, in larva of Dytiscus,
1273

Eye -stalk, formation of, in Astacus, 184,
189 ; in Loligo, 357

Fascia of muscles, formation of, mAmp/uo,i-us
lanceolatus, 599

Fat body, formation of, in embryo of
Donacia, 256 ; in embryo of Scolqpendra,
283

Fat cells in embryo of Agelena, 227

Female, definition of, 2

Female proimcleus, 9

Fertilization of egg of Cynthia partita, 611

Filament plate, formation of, in I'ftyUodromia,
263

Fin-ray cavities, formation of, in larva of
Amphioxus lanceolatus, 599

Fin-rays, formation of, in A»ipln<>.i-nx lunceo-
latus, 599

Fiona, 320, 321, 323, 324

First maxilla of Astacus, 186

First maxillary segment in Donacia, 252

First polar body, definition of, 9

First somatoblast, formation of, in Dreis-
sensia, 333 ; in Nereis, 155 ; in Nephelis,
160

Fissurella, 300, 304, 320 ; metamorphosis
of larva of, 305

Fixation, definition of, 39 ; of larva of Ante-
don rosacea, 548 ; of Brachiolaria larva of
Asterias, 409 ; of larva of Antenna gibbosa,
473 ; of larva of Clatlu-liin, 47 ; of larva
of Bsperia, 45 ; of larva of (•'r/i/it/n, 39-
41 ; of larva of Leucosolena, 47 ; of C'ypho-
nautes larva of Mei/ihru ni/>om, 394 ; of
larva of OscareUu, 41 ; of larva of Phy-

lactolaemata, 396 ; of larva of Sponyilla,

47
Fixation pit of larva of Antedon ros«<-t-<>.

formation of, 547
Fixed cheek in Trilobite larva of Litnulvs,

238
Fixing disc of larva of Antedon rosacea, 551 ;

of larva of Asterias, 469 ; of larva of

Asterina gibbosa, 473
Flabellum of Limulus, 237
Flemming's fluid, composition and use of, 33
Flies, larvae of, 25

Float, development of, in Siphonophora, 66
Floscularidea, 418
Flustrella, larva of, 395
Follicle cell, definition of, 3
Food -yolk, 19; definition of, 3. (See

Deuteroplasm.)
Foot, formation of, in Dentalium, 329 ;

in Dreissensia, 342 ; in Paludina, 314,

323 ; in Patella, 299 ; in Trochus, 323
Foot-gland, formation of, in Callidina rtis-

seola, 425
Foot-plate, formation of, in larva of Antedon

rosacea, 551
Foot segment in larva of Tercbratulina sep-

tentrionalis, 411

Fore-foot, formation of, in Loligo, 358
Formalin, use of, 33
Formation of layers, definition of, 27 ; in

Crustacea, 191-196 ; interpretation of, 659
Formative stimuli in eggs of Echinoidea, 528,

529
Free cheek in Trilobite larva of Linmhix.

238

Frontal field in larva of Asterias, 464
Frontal filament in Nauplius larva of Cirri-

pedia, 202

Functional continuity, law of, 66
Funnel of uephridium of Criodi'ilux lacinim,

formation of, 159 ; in Ctenophora, 561 ;

completion of, in Loligo, 362 ; formation

of, in Loligo, 357

Galerucella, 271, 272, 277, 280

Galerucetta ulmi, metamorphosis of, 267-270

Gamete, definition of, 2

Gametogenesis, definition of, 2

Ganglion, formation of, of adult Cionn ///-
testinalis, 622 ; of Donacia, 252

Gastral filaments, formation of, in Auirlia.
71

Gastral groove in embryo of Donacia, 250 ;
closure of, in embryo of Donacia, 253

Gastropoda, 291, 504, 651 ; ancestors of,
368, 369 ; development of, 290-324

Gastro-vascnlar canals of Ctenophora, 561

Gastrula, definition of, 68 ; interpretation of,
661 ; of Anti'Jon rosacea, 545 ; of Ascaris
megalocephala, 443, 444; of Astacus, 180;
of Asterias, 460 ; of Asterias, experiments
on, 483; of Aurelia, 68; of Balanoglossus
darii/i'i'iift, 571 ; of Cerelirnf ul 11* lacteus,
120; of Ech inusesculcntus, 507; of Mt«'r»-

INDEX

G7T

biotus, 243 ; of Afembranipora, 388 ; of
Newt, experiments on, 660 ; of 1'olu-
dina, 310 ; of Pedicellina echinata, 399 ;
of Peripatus cafiensis, 171 ; of Pol;/-
gordius, 132, 139 ; of Sagitta bipunctatu,

429 ; of Synapta digitata, 531 ; of Tere-
bratulina septentrionalis, 409 ; of Urticina
crassicornis, 77

Gastrulation in embryo of A mphioxus lanceo-
latus, 589 ; in embryo of Ascaris meyaloce-
phala, 444 ; in embryo of Aurelia, 68 ;
in embryo of Callidina russeola, 422 ; in
embryo of Cynthia partita, 616, 617 ; de-
fined, 68 ; in embryo of Dentalium, 328 ;
in embryo of Dreissensia, 335 ; in embryo
of Patella, 295, 297 ; in Peripatus capensis,
171 ; in embryo of Phascolosoma, 375 ;
in embryo of Urticina crassicornis, 78

Gemmule of Spongilla and Ephydatia, 47

Generative cell, formation of, in Polyphemus,
194

Genital bnrsa of Aiiiphium squamata, as
womb, 484 •

Genital cells, development of, in Ascaris
megalocephala, 443 ; in Donacia, 257 ; in
Loligo, 358 ; in Sagitta bipunctata, 429,

430 ; in Tubularia, 58

Genital coelom, formation of, in Loligo, 364

Genital dnct, formation of, in Agelena, 230 ;
in Astacus, 189 ; in Asterina gibbosa, 481 ;
in Paludina, 316 ; in Peripatus capensis,
175 : in 8<-<>l»i>i'ndm, 283 ; of Scorpion,
241

Genital folds, formation of, in Loligo, 364

Genital operculuin, formation of, inLimulus,
238 ; in Scorpion, 241

Genital organs, development of, in Agelena,
230; mAmphioxuslanceolatus, 600-601; in
A ntedon rosacea, 558 ; in Astacus, 189; in
Asterina gibbosa, 480 ; in Oallidinarusseola,
424 ; in Cucumaria glacialis, 540 ; in Dreis-
sensia, 337, 346; in Echinus esculentus, 521 ;
in Limit! KS, 236 ; in Loligo, 364; in Macro-
biotits, 243 ; in Mulgula, 628, 629 ; in
Pohulina, 316; in Peripatus capensis, 17 5;
in Phyllodromia, 262 - 263 ; in Sagitta
bipimctata, 433, 434 ; in Sc<.iloj}etttli-n,
283 ; in Scorpion, 240 ; in Synapta riri-
para, 539, 540 ; in Tornaria of Nassau,
581 ; in blastozooid of Urocliorda, 639

Genital plates, formation of, in Echinus
esculentus, 516

Genital rachis, formation of, in Aiupltini-n
squamata, 501 ; in Asteriim <///'/" «", 481 ;
in Echinus esculentus, 520

Genital ridge, formation of, in Donacia, 256 ;
in Phyllodromia, 263

Genital stolon (see also Dorsal organ), forma-
tion of, in Amphiura squamata, 500 ; in
Asterina gibbosa, 480; in EcJiinus escu-
lentus, 516

Gephyrea, 163, 401, 416

Gephyrea nnda, 372

Gephyrea tubicola, 372. 380

Germ-layers, definition of, 27

Germarium of diJIiilhin /-//x.siWj/, 424

Germinal disc, see Embryonic arm

Germinal spot, definition of, 3

Germinal vesicle, definition of, 3

(Ji-ri/mnn, experiments of eggs of, 96

Geryonidea, development of, 67

Gill, development of, in Astacus, 189 ; in
343 ; in Loligo, 357 ; in
i, 315 ; in Salpa, 636 ; early
formation of, in Cephalopoda, 369 ; late
formation of, in Gastropoda and Pelecy-
poda, 369

Gill-books, formation of, in Limnlus, 238

Gill-pouches, formation of, in New England
Tornaria, 577

Gill-slit, first, formation of, in larva of Am-
2>hioxus, 596

Gill -slits, formation of, in larva of simple
Ascidiau, 620 ; in embryo of l'i//'<>x<nii</,
634

Glabellum in Trilobite larva of Limulus, 238

Glacial acetic acid, use of, 33

Glandular cells of larva of Galerucella tdmi,
metamorphosis of, 268

Glandular pockets of mid-gut in lionacia,
255

Glandular tube of larva of Achtheres amb/n-
plitis, 207

Glass body of ocelli of Dytiscu*, 274

Glass-crab, 214

Glochidium, 655 ; larva of Unionidae, 350

Glockenkern of Medusa of Tubidaria, 58

Ulossiphonia, 161

Guathites, formation of, in ancestors of
Arthropoda, 244

Gnathobdellidae, 128, 160, 163, 184

Gonangium, definition of. 63

Gonidial groove of Actiuozoa, definition of,
83

Gonocoele, definition of, 166 ; formation of,
in Amphioxus lanceolatus, 587, 601

Gonophores of Clam, 62 ; nf Cordylophora,
62; of HaleciuiD, 62; of Sertularia, 62;
of Ti'buliirii.i, 54

(,'<i/-i/<i/-i<i, 86

Grantia, 43, 44, 46, 47, 51, 52 ; develop-
ment of, 37-43

('i-nn/tii cmiipressa, 37

Grub of Donacia, 260 ; of Doryphora, 261

Gut, development of, in Amphioxus lanceo-
/nf us, 595; in Antrdmi rosacea, 547; in
larva of Aftertax, 461 ; in Cerebratuius
In, -ti'ii.-;, 120; in <'i-H>,Yll<i oculata, 481;
in Snitiff" I'i/inni-hiln, 4:il ; in Sola
endeca, 482 : in ]',•,•> i'/-nfi'/ in" septentrion-
alis, iui'

Gyminilila^tca, 53

Gyninolaemata, 386

Haematoxylin (Givnaclu-r'.s), advania-t-s of,

35
Haemocoele of Peripatus capensis, fnnuation

of, 172

678

INVERTEBKATA

Haled urn, 62

Haliotis, 301, 304, 320 ; metamorphosis of

larva of, 305
Hatschek's nephridmm, formationof, in larva

of Amphioxus lanceolatus, 600
Hatschek's pit, formation of, in larva of

Amphio.vus lanceolatus, 596
Head blastema, formation of, in Xephelis,

162 ; in Phascolosoma, 375 ; in Poly-

gordius appendiculatus, 147
Head of spermatozoon, definition of, 7
Head-cavities, formation of, in larva of

Amphio-i'iis hi/iceolatus, 595 ; in Sagitta

bipunctata, 431
Head-kidney of New England Tornaria,

formation of, 577

Head-pouch of larva of Muscidae, 278, 279
Head - segment of larva of Tercbratiilinn

septentrionalis, 410
Head-shield in Astacus, 185
Head-vesicle of embryo of Dnio, 351
Heart, formation of, in Agelena, 229 ; in

Astacus, 187 ; in dona intcstinalis, 626 ;

in Donacia, 257 ; in Dreissensia, 344 ;

in Liinulus, 256 ; in Loliyo, 362 ; in

PaluJina, 314 ; in Peripatus capensis,

174 ; in Cyathozooid of Pyrosoma, 634 ; in

Scorpion, 241 ; in New England Tornaria,

575

;/<•/,>, yolk-sac of, 369
Hemiaspis, 239

Hemichorda, 568 ; development of, 569-586
Hemimetabola, 245, 277, 287, 288
Hemiptera, 245, 277
Heredity, Weismann's theory of, 12
Hermann's fluid, composition of, use of, 33
Hermaphrodite, definition of, 2
Hermelliformia, 128
Heterochromosome, 14
Heterochrouy, 608 ; definition of, 46 ; in

development of Cephalopoda, 370
Heterocoela, 37
Heteronemertini, 118 ; development of, 118-

126

Hexactinellida, 37 ; development of, 43
Hexactiniae, 53, 83, 86, 87
Hexapoda, 285

Hieraciinit, asexually reproduced, 18
Hind-foot, formation of, in Loligo, 357
Hirndinea, 128 ; development of, 159-163
Histogenetic plasm, definition of, 13
Histolysis of Cyphonautes larva in meta-
morphosis, 394
Holoblastic, definition of, 26
Holometabola, 245
Holothuria tubulosa, 530 ; development of,

541
Holothuroidea, 287, 456, 464, 545, 560,

•564, 565, 585, 656; pupa of, 28; develop-
ment of, 529-544
Homarus, 178, 191, 213
Homocoela, 37

Hooks, disappearance of, in PlMscolosoma
379 ; formation of, in arms of

Ophiothrix fray His, 498 ; in Phascolosoma,
379 ; in Kayitta bipunctata, 433

Hoplocarida, 177

Hormones, 652

Horse-shoe Crab, 221

Hybrids of Echinus esculentus and Echi no-
card i um cordat.um, 523 ; of Echinus escu-
lentus and Echinus miliaris, 523

Hydra, 63, 64, 69, 70, 88, 383 ; egg of, 27

Hydra-tuba, 70, 79, 80

Hydrida, 53

Hydrocoele, formation of, in embryo of
Antedun rosacea, 547 ; in larva of
Asterias, 466 ; in larva of Asterina
gibbosa, 474 ; in larva of Oribrella oculata,
481 ; in larva of Echinus esculentus, 510 ;
in larva of Ophiothrix fragilis, 491 ; in
larva of Ophiura brcvispina, 501 ; in
Solaster endeca, 481

Hydroides, 313

Hydromedusae, 53, 62, 64, 66, 67, 69, 72,
98, 126

Hydrophyllium of Siphonophora, 66

Hydrothecae, definition of, 62

Hydrozoa, 53 78, 79, 96, 161, 659, 661 ;
development of, 54-67 ; development com-
pared with that of Scyphozoa, 74-76

Hylodes, development of, 22

Hymenoptera, 245, 266, 386

Hyocrinus, 559, 560

Hypertonic solutions, use of, 17, 18

Hypogastric coelomof Asterina gibbosa, 475,
480

Hypopharynx, formation of, in Donacia, 252

Hypophorella e.'.'pansa, larva of, 394

Hypophysial canal, formation of, in larva
of simple Ascidian, 622 ; in blastozooid
of Urochorda, 639

Hyposphere in larva of Polygordiiis, 140 ;
disappearance of, in larva of Polygon! ins
appendiculatus, 149

Id, definition of, 13

Iiliochromosome, 14, 15

Idiosome of spermatozoon, definition of, 7

Ilyanassa, 332

Imaginal disc for compound eye of Dytiscus,

275 ; for adult oesophagus in Polygordiiix

appendiculatus, 149
Imaginal discs in larva of Galerucetta ulini,

267, 268 ; in larva of Muscidae, 278 ; in

Pilidium larva, 122
Imaginal pouches for wings and legs in

Muscidae, 279
Imaginal ring for proctodaeum of larva of

Muscidae, 279 ; for salivary glands of

Muscidae, 279 ; for stomodaeum of larva

of Muscidae, 279

Imago of Donacia, 260 ; of Echinus escu-
lentus, 517 ; of Galerucella ulmi, 268
Immersed embryonic area in segmenting egg

of Lepidoptera, 266
Inbreeding, definition of, 18
Indeterminate cleavage, definition of, 416

INDEX

679

Iiifundibnluin of Ctenophora, 561
Iiihalent pores of Grant ia, formation of, 43
Ink-gland, formation of, in Luliyu, 358
Inner segment of lens, formation of, in

Cephalopod eye, 366

Insecta, 169, 177, 204, 281, 282, 284, 285,
652, 662 ; embryonic development of,
245-266 ; metamorphosis of, 266-280
Insecta Hexapoda, 245
Instar, definition of, 19
Intercalary segment in embryo of Donacia,
252 ; in embryo of L<'ji!sina, 265 ; in
embryo of Scolopenctra, 282
Intermediate cells of Molluscan cross in

embryo of Patella, 294
Intermediate dorsal arms of ciliated band in

larva of Si/napta iU<jitat«, 533
Intermediate girdle-cells, degeneration of, in
larva of Polyyonliu.s appendiculatus, 149 ;
formation of, in embryo of Phascolosoma,
374

Internal madreporite, formation of, in An-
tarctic Cuci/niaria, 542 ; in Synapta
diijitata, 539
Internal perihaemal ring-canal, formation of,

in Asterina gibbosa, 475
Internal sac in Cyphouautes larva, 390, 392
Internal yolk-sac, formation of, in £(<//,</",

360
Inter-radial cells of embryo of Poli/gordii'.-',

135

Inter-radial lobe of stomach of Aureliu, 71
Inter-radius in egg of Polygordius, 135
Intestine, formation of, in Anti '</</// rosacea,
552; in larva of .!*/-•/•»/*, 462; in larva
of Asterina gibbosa, 472 : in larva of
Balanoglossus clavigerus, 573 ; in ])en-
talium, 328 ; in Dreisxensiu, 337 ; in
larva of Echini's esculent us, 508 ; in adult
Echinus esci'.lent'its, 520 ; in Loligo, 364 ;
in larva, of Membranipora, 390; in larva
of Ophiotforix fragilis, 487; in larva of
Peilicclliini t'l'/ii/tii/K, 400 ; in larva of
Synapta digitata, 532

Introvert of Phascoh>si.nnu, formation of, 379
Imagination in eggs of Astacus, 181
Invertebrata, 662 ; embryology of, 30
Iris, formation of, in eye "t /.»//:/<', 363, 367
Islands of embryonic tissue in mid-gut of

larvae of Mnscidae, 279
Isoplenra, 291
Isopoda, 22, 177, 193, 219

Jaws of Echinus I'scti/en/nx, formation of, 520
Jaw-region of embryo of Donacif, 251
Jaw-segments in embryo of Scu/njn ml rii, 282
.1 ii I us, development of, 284

Karyokiuesis of zygote, 9, 10

Kidneys (see also Excretory organ and
Nephridinm), formation of, in Dreissensia,
343 ; in Loligo, 362 ; in Paludina, 314 ;
in Perijintus capensis, 174 ; in Unin, 353

Krohniv, 428

Labial palps, formation of, in Dn :i*.^ :u*in.

344
Labrum, formation of, in Asfftciix, IS.'!; in

l>oiiiii'iij, 252

Laeotropic cleavage, definition of, 105
Laniellibranchiata, 291
Laoilice, experiments on the eggs of, 96

Larva, definition of, 19

Larva of Amphio.n'a lanceolatus, 593-600 ;
of Anti-linn I'usni-i'K. 517-553: of simple
Ascidian organization of, 619-622 ; of
Asti-rinn i/i/iln'Sii, 472-477 ; of Coleoptera,
287 ; of Vribrella ocnfitln, 481 ; of Cucu-
maria /'/<'//<•/, 542 ; of Desor, 118 ; of
Dolii-liiiijliiaan.-i kowalevskii,582; oll>ulii-lio-
glossus pi'sillus, 583 ; of Domn'in, 200 ;
of Echinodermata, 287 ; i-i<ili-i-ii,;ll<i ulmi,
207 ; of lusecta, interpretation of, 286-288 ;
of Jnliis, 284 : of Lepidoptera, 266 ; of
Muscidae, 278 ; of Uphinrn Inn-lap! HH,
502 ; of Pantopoda, 243 ; of Pentastomida,
242 ; of Sagitta iiipn m-tula, 433 ; Solaxti r
endeca, 481, 482 ; of Terdn-nti'l! nn septen-
li'ionci.lis, 412

Larvacea, 568, 608, 646

Larval adductor muscle of Unio, 352

Larval arms of Asterias, 464 ; of Balano-
glossus, 576 ; of Ei-liiiini-iiniiiijn cordatum,
522 ; of EfliiiiHx esculentus, 508-511 ; of
riKji/in. 488-490; of Symij>/i>
i, 533

Larval cerebral ganglion of J'iili/gnr<Uii.i
appendiculatus, 147

Larval eyes in grubs of Duryplini-n and
Donacia, 261 ; in grubs of Di/fixca*, 273,
274

Larval history of Auomura, 216 ; of
Crustacea, 196-220

Larval kidney, formation of, of Apli/ain, 32-1 ;
in Dreissensia, 340 : in Fioiu', 324 : in
Opisthobranchiata, 323, 324 ; in Paludina,
310, 323 ; in Physa, 323 ; in fresh-water
Prosoliranchiata. 323 ; in Pulmonata, 32-". :
in Umbrella, 324

Larval mantle of Unio, modification of, 352

Larval mesoderm of /Jf>///.</«/v7//'.s-, 135; "I
Mollusca, 323

Larval phase, definition of, 19; intn juria-
tion of, 649

Larval shell of Acniam, 304 ; of Fiaann-lln.
305; of Hiiliiites, 305 ; of M<-nil<f« i<ii>»f<i,
392 ; of Puffin, 300

Larval skeleton, development of, in AI/IJ>/H'-
ura squamata, 198: u\£i-li!nii.->-*
508-510; mOphiothrixfragilis, 1^7-490

Larval stages, dftinil ion of, 19

Lateral chamber of Urticina orassicornis,
80

Lateral eyes, formation of, in i . 232

2-">4 : in Limulus, 2".7 : in Sn.rpimi, 240

lateral muscles "I <'y]ihonaiites larva, 393 ;
of /'iifi/'/tiriJin* appendicula u . L48

Lateral nerves of larva of
app( ndiculatus, 1 17

680

INVEKTEBKATA

Lateral plates, formation of, in Amphiura

squamata, 499
Lateral sinus, formation of, in Peripatus

capensis, 174

Lecithin, ingredient of food-yolk, 3
Leda, 349
Left anterior coelom of larva of Asterias,

466 ; of larva of Echinus esculentus, 509 ;

of larva of Ophiothrix fragilis, 490
Left posterior coelom of embryo of Antedon
rosacea, 547 ; of larva of Asterias, 466,

468 ; of Echinus esculentus, 509, 514,

515 ; of larva of Ophiothrix fragilis, 490,

494
Legs, formation of, in Julus and Scolopendra,

284

Legs of Donacia, jointing of, 252
Lens, formation of, in compound eye of

Astaciis, 189 ; in eye of Cephalopoda,

366, 367 ; in ocelle of Ijytiscus, 274 ; in

compound eye of Dytiscus, 276
Lepas, embryonic development of, 195
Lepidoptera, 245, 266, 272, 278, 286, 288
Lfjiidosiren, maturation of male cells of, 4
Lepisma, development of, 263, 264, 266,

282, 286

Lepralia, corona of larva of, 395
Leptinotarsa decemlineata, development of,

245, 246, 247

Leptogorgia virgulata, development of, 87
Leptonema, definition of, 4
Leptostraca, 177

Leptotene thread, definition of, 4
Leuconidae, 37

Leucosolenia, 43 ; in development of, 47
Limnaea, 323
l.inuilus, 221, 241, 244, 282; development

of 236-239
lAngula, 414
Lip-cavities, formation of, in Amphin.'-i<s

lanceolatus, 606

Liriope, experiments of eggs of, 96, 97
Lithium larva of Echinoidea, 526, 527, 528
Liver, formation of, in Agelena, 235 ; in

Astacus, 190 ; in Dreissensia, 337 ; in

Loligo, 364 ; in Paludina, 315
Lobata, 53

Loligo, development of, 356-366
Loligo vulgaris, 353
Longitudinal ciliated band of larva of

Asterias, 463 ; of larva of Balanoglossus

rlm-iyerus, 574 ; of larva of Echiuoidea,

464 ; of larva of Echinus esculeittus, 508 ;

of larva of Ophiotliri.f fragilis, 487 ; of

larva of Synapta digitata, formation of,

532
Longitudinal muscles, formation of, in

Amphioxus lanceolatus, 594 ; in Oriodrilus

/>tci ma, 158 ; in larva of Cynthia partita,

615 ; \\-iPolygor<lii/s appendiculatus, 147
Lopadorhynchus, 1
Lophophore of Brachiopoda, 407
Lophophore of Terebratulina septentrional is,

development of, 413

Loricata, 177

Loricata, larval history of, 214

Lower layer cells, formation of, in segment-
ing egg of Sepia, 356

Lower sclerotomes, formation of, in Amphi-
oxus lanceolatus, 599

Loxosoma, 398

Lucifer, 177, 192, 203

Lnidia, 457

Lumbricus, 157

Lung-books, formation of, in Scorpion, 241

Lung-sac, formation of, in Agelena, 231 ; in
Scorpion, 241

Lycosa, 221

Lysin, 17

Machilis, 284, 286, 287 ; development of,
265, 266

Afacrobiatus tnacronyx, development of, 243

Macromeres in segmenting egg of A mphioxus
lanceolalus, 588 ; in segmenting egg of
Beroe, 90; in segmenting egg of Dentalium,
327 ; in segmenting egg of Dreissensia,
333 ; in segmenting egg of Echinus escu-
lentus, 506 ; in segmenting egg of Patella,
293 ; in segmenting egg of Phascolosoma,
373 ; in segmenting egg of Planocera,
104

Macro-segments of Donacia, 251

Macrura, 177, 208, 210

Madreporic pore, formation of, in larva of
Antedon rosacea, 547 ; in larva of Asterias,
465 ; in larva of Echinus esculentus, 508 ;
in larva of Ophiothrix fragilis, 489 ; in
larva of Synapta digitata, 531

Madreporic vesicle, formation of, in Asteriux,
467; in Asterina gibbosa, 467, 474; in Crib-
rdla ociilata, 481 ; in Echinus esculentus,
511 ; in Ophiothrix fragilis, 492 ; in
Solaster eiuleca, 481

Malacostraca, 177, 655

Male, definition of, 2

Male-cells of A scar is megalocephala, 439

Male prouucleus, definition of, 9

Malpighian tubes, formation of, in Agelena,
230 ; in Donacia, 260 ; in Scorpion, 240 ;
metamorphosis of, in larva of Galerucella
ul mi, 270

Mammalia, 657

Man, young of, 19

Manchette, 7. (See Ruffle. )

Mandibles, formation of, in Astacus, 184 ; in
Cyclops, 199

Maudibular cavities of Vertebrata, 606

Mandibular segment in Donacia, 252

Mantle, formation of, in simple Ascidian,
622 ; in embryo of Membranipora, 389 ;
in Pedicellina echinata, 403 ; in adult
Unio, 352

Mantle-cavity, .formation of, in Jtreisxciisitt,
339 ; in Loligo, 357 ; in Patella, 300

Mantle-fold, formation of, in Jlentalium,
329 ; in Paludina, 315 ; in Patella, 300;
iu Terchriitnl inn septentrionalis, 410

INDEX

681

Mantle-groove, formation of, in Palttdinn,

314

Mantle-layer, definition of, 63
Manubrium of medusa of 1'odocoryue, 61 ;

of Tubitlaria, 58
Mastax, formation of, in Callidina russen/'i,

424
Maturation, divisions of germ-cells, 3 ; of

egg, in Crepidula, 7, 8 ; of spermatozoon,

in Lepidosiren, 4-6
Maxillipedes, development of, in larva of A ch-

theres amblojrtitis, 207 ; in Astaciis, 186 ;

in Mysis larva- of Crangonidae, 215 ; in

Cyclops, 197
Mayer's fixative, 35
Median dorsal arm of ciliated baud of larva

of Asterias, 464
Median retractor muscle of larva of Dreis-

sensia, formation of, 341
Median ventral arm of ciliated band of larva

of Aster ins, 464
Medullary folds, formation of, in ijmbryo of

< 'inithia jiartita, 619
Medullary plate, formation of, in embryo of

^Imp/tiiixus lanceolatiis, 591
Medusa-buds (see Gonophore) of Siphono-

phora, 66; of Tubularia, development of, 57
Medusae, free, development of eggs of, 59-

61

Medusome theory of Haeckel, 66
Megalopa larva of Brachyura, 216
Melicertidea, 418
Mi II! tn tcxtndinata, 504, 522
Milnlontha, 287 ; abdominal appendages of,

266

Membranipora, development of, 387-394
Membranipora pilosa, 387
Meridional canals, formation of, in Beroe, 94
Meroblastic segmentation, detinition of, 26 ;

in eggs of Arthropoda, 178 ; in eggs of

Cephalopoda, 178, 353 ; in eggs of Pera-

carida, 193 ; in eggs of Pyrosoma, 632 ;

in eggs of Scorpion, 240 ; in eggs of Sepia,

353
Mesectoderm in Annelida, Mollusca, and

Gephyrea, 401 ; formation of, in Lepas,

195 ; in Mollusca, 323 ; in Patella, 309 ;

in Phascolosoma, 376 ; in Planoccra, 111 ;

in J'nli/r/orilii/x, 135
Mesi'iichyme, definition of, 120 ; formation

of, in embryo of Antedon rosacca, 545 ;

in larva of Asterias, 461 ; in larva of

Balanoglossus davigerns, 573 ; in larva of

Cerebratulus ladeus, 120 ; in larva of Cn-

cui/iaria planci, 542 ; in larva of Cynthia

partita, 614 ; of (irantia, 39 ; in larva

of Holothuria tubidosa, 541 ; in larva

of Oji/i/iira liivri.ipiiia, 501 ; in larva of

Pediccllina echinata, 401 ; in embryo of

Pyrosoma, 635 ; in larva of N//"'V'/"

d if/i fata, 531
Mesendoderm. formation of, in C'/v// !<lnla.

323 ; in ])i-cixx<-iix!a. 335 : in Fiona, :J23 ;

in I'ln/xa, 323 ; in Sepia, 356

Mesellterie stomata of I'rtn-'nni ow .Wen /•///.•>•,
SO

Mesenterial filaments oiUrticina cras.iicornis,
81

Mesentery of Crlif/na <Ta.xxi<-n,-nix. 79

Mesoderm, formation of, in Agelena, 224 ;
in Alcyonidiii ni it/liiihmi, 388 ; in .lm/i/ti-
oxus litiii-i'iilatns, 592; in Astacnx, 180;
in Beroe, 93 ; in B/at/a, 261 ; in Cri'
322 ; in Donacia, 248 ; in
335 ; in Enjilianxiii, 192 ; in Fiona, 322 ;
in Lfjxis, 195 ; in Linudus, 236 ; in
Nephelis, 161 ; iu Oligocliaeta, 156 ; in
Pallenc, 243 ; in Paludina, 310 ; in
Patella, 295 ; in Pedicelliiw, 399 ; in
Pedipalpi, 241; in Phascolosoma, 375;
in Phyxa, 322 ; in P/anocera, 108 ; in
Polygordius, 143; in Poli/ji/n'mns, 194;
in Salpa, 636 ; in Scorpion, 240

Mesodermal bands, formation of, in A<tfli'na,
225 ; in Den fa./i-nni, 329 ; in Lepas, 195 ;
in Lepisma, 265 ; in Oligochaeta, 156 ; in
Palmlina, 310 ; in Patella, 299 ; in
Pedicel Una echinata, 401 ; in Peripatns
I'upensis, 171 ; in Polygordius, 138 ; in
Poli/gordins appe/ulicidatns, 144 ; in
Scolopendra, 283

Mesogloea of Urticina crassicornis, 79

Mesomeres in egg of Ecln'iu/.t rsridt.'i/fti.i, 506

Mesonemertini, 118

Mesotrochal larva, definition of, 153

Metamorphosis of Copepod id larva of .-1 chfheres
amblnjilitin, 207, 208 ; of larva of Amji/n'-
oxus lanceolatiis, 603, 604 ; of larva of
simple Ascidian, 622; of larva of As-
terias, 467-472; of the larva of .l^/V/ •///</
gibbosa, 474-479 ; of Zoaea larva of
Brachyura, 215 ; of larva of (Jiiuta intesti-
iialix, 622-628 ; of pupa of Cirripedia,
202 ; of Mysis larva of Crangouidae, 2] 5 ;
of larva of Cyclops, 198, 199 ; of larva of
Dreissensia, 343; of larva of Ei-liim'*
esculentus, 512-518 ; of Insects, 266-280 ;
of larva of M<:/iilu-n ni/mra. 394 ; of larva
of Ophiothrix fraffilis, 492-498; of larva
of Ostracoda, 203 ; of larva of Pedi<-rllina
echinata, 402, 403 ; of larva of 7V»>W..-
xfiiiia, 377, 378; of larva of Plmi'miix
(Actinotrocha), 383, 384 ; of larva of
Polygordius n/>i>< •/////< niahix, 1 49-151 ; of
larva of Xi/na/ita iliijitnta, 5:ir.-."ill ; of
larva of Terebratulina septentrionalis, 112,
41o ; of New England Tornaria larva,
577-579 ; of NMSSIHI Tornaria larva, 580,
581 ; of the larva of Yum/la ! Tilidium),
112-115

Mi'taliauplins lai'va of I 'i^-tajix, 1!*S; of
Stonia1o]ioila, 216

Metanauplius stage in develojiiiii'iit of
Achtheres am/i/ii/iti/ix, 206

Metanemertini, 118

Mctanephridia. formation of, in Polygordius,
147

i-is, ih-tinilioii of. 12

682

INVEETEBEATA

Metatroch of larva of JJreissensia, 340 ; of
larva of Phascolosoma, 376 ; of Actino-
trocha larva of PAorom's, 381 ; of larva of
Polygonlivs, 140, 144 ; of adult Polyzoa
Ectoprocta, 386

Metazoa, 51, 100, 170 ; ancestry of. 116, 660

Metazoaea larva, 213

Method of finding eggs of ItoUchoglossus
kowalevskii, 582

Methods of reconstructing sections, 319

Met rid in a i marfiiiuit ii in, 85

Micromeres in segmenting egg of -1//^A /".>•//*
lanceolatus, 588 ; in segmenting egg of
JBeroe, 90 ; in segmenting egg of Dentalivm,
327, 328 ; in segmenting egg of Dreissensia,
333, 334; in segmenting egg of Erliini'x
esculentus, 506 ; in segmenting egg of
Patella, 293-295 ; in segmenting egg of
Phascolosoma, 373, 374 ; in segmenting
egg of Planocera, 104

Mid-gut, formation of, in Agelenu, 230 ; in
Astu.cus, 189 ; in Donacia, 254 ; uiJvlus,
284 ; in Loligo, 358; in Scolopendro, 284;
metamorphosis of, in larva of GaleruceUa
ulmi, 269

Middle piece of Spermatozoon, definition of. 7

Miguel's solution, 131

Millipedes, 281

Mites, 242

Mitrocrima, experiments on eggs of, 96

Molgula, 628

Moli/ulii ii,iii>nU<ii<les, development of, 632

Mollusca, 105, 108, 157, 372, 400, 401, 405,
406, 408, 413, 416, 427, 435, 436, 457,
523, 529, 561, 562, 651, 655, 659, 661 ;
development of, 291-371 ; development of
unfertilized eggs, 17 ; eggs of, 9 : fossil
representatives of, 20 ; sperm of, used to
cross-fertilize eggs of Sea-urchin, 17

Molluscan cross, definition of, 133 ; in seg-
menting egg of <_'irj»'(hila, 322 ; in seg-
menting egg of r<ilrll«, 294 : in srgmtnt-
ing egg of Phascolosoma, 374 ; in segment-
ing egg of Pobjijordhis, 133

Molluscoida, 60S'

Monotrochal larva, definition of, 153

Monotus, 115

Monovalens race of Ascaris megaloceplinln
439

Morula of Tubular ia, 54, 55

Mouth, formation of, in A/iiphio.cim lanceo-
lii.tits, 596 ; in simple Ascidian, 619 ; in
Astacus, 183, 184 ; in larva of Asterias,
461 ; in adult Ax/a-ias, 471 ; in adult
Ast, ',-i,in ///////,«</, 479 ; in adult Echinus
esculentus, 518, 519 ; in adult Ojihinthi-l.i-
fragilis, 495 ; in 1'nlinliiia, 310 ; in Peri-
patus capensis, 171: in 7VW« /•/</, 56;
function of, in Platyhelminthes, 102

Mouth in Aurcfia identical with blastopore
68

Midler's fluid, composition of. use of, 33
Miiller's larva, 104, 164 ; compared to a
Ctennphoiv, 115

Mailer's papillae, formation of, in larva of

Arilp]lil>.:-IIS /</,/C,_;:/</fl'S, 604

Musca, 280

Muscidae, 272, 278, 287 ; metamorphosis
of, 278-280

Muscles, formation of, in Antedon rosacea,
558 ; in Callidina russeola, 426 ; in
Pilidium larva of Cerebratulus ln.ctcus,
120, 121 ; in Cyphouautes larva, 390, 391 ;
in arms of Ophiothrix fragttis, 498; in
stomodaeum of Ph/mvcra, 111 ; in blasto-
zooid of Urochorda, 639 ; in Urtidna
crassicornis, 83 ; metamorphosis of, in
larva of Galcrn<;-U,i ulmi, 270

Myoblasts of JTej >//clis, 162; of Criodrilns.
158

Myocoeles in Ainphio.''//* /tin<'eolatnx, 601

Myotomes, formation of, in Amji/iiu.,-,^
lanceolatus, 595

Myriapoda, 169, 177, 245, 285; development
of, 280-284

Mysidacea, 177, 219

Mysis, 193

Mysis larva, 213, 217 ; interpretation of,
213 ; of Astacidae, 213 ; of Crangonidae,
215 ; of Loricata, 214 ; of Thalassiniclae,
215

M/iiilm, 332, 523

Narcomedusae, 53 ; development of, 66, 67

Xauplius lavv;i, I'S''. 054, 655 : interpreta-
tion of, 204, 205 ; of Apus, 201 ; of
Branchiopoda, 201 ; of Cirripedia, 201 ;
of Cladocera, 200 ; of Cyclop, 196-197 ;
of Euphausidacea, 203 ; of (.)str:icoda,
203 ; of Penaeidea, 203 ; of Penaeus, 22,
of Saco/lino, 202; of Stomatopod;i. 217

Nauplius - like ancestor of Crustacea, 205,
212

Nauplius stage in development of At-l/tlicrcs
ambloplitis, 206 ; of A slac-us, 185

Xat'titus, 358 ; motion of, 369

Neanic st.-igi- of development, 19, 22

Nectocalyx of Siphonophora, 64, 66

Nematoda, 436, 457 ; development of, 437-
455

Nemertiuea, 157, 164, 166, 167, 457, 529,
561, 600, 661 ; development of, 118-127

Nephridia, formation of, in Amj>hio.c»s
lanceolatus, 600 ; in Criodrihts lacvtnn,
158 ; in Xi'pJtclis, 162 ; in Pluixi-aliismiKi,
379, 380 ; in Actinotrocha larva of Ph»i--
onis, 381, 382 ; nature of, in Annelida,
157

Nephridioblasts of Jfejihefis, 162

Xi'pln-i'px, 213

Nephropsidea, 177

Nephrostome, formation of, in Phascolosomn .
380

Nereidiformia, 128, 1 .">:'.

JTereis, 129, 153, 156, 321, 333, 645;
development of, 155, 156

Nerve-collar of PolygoTdius appendiculatus,
formation of, 147

INDEX

683

Nerve-cord, formation of, in Phascolosoma,B77

Nerve-ring; formation of, in adult Ant<:<l<>n
rosacea, 554 ; in Cuci'mi/i-ia /i/n/icf, 542

Nervous system, formation of, in A g<-/, ,/n,
226; in embryo (and larva) of Antedon
rosacea, 547; in Astoms, 184; in adult
Asterinagibbosa, 477; in larva of 1)«1 /«//'///,
637 ; in ])»iuiclii, 257, 258 ; iu larva of
Ec/iiit/txi'xni/eiifiiK, 516 ; in adult Ech inns
esculentvs, 574 ; in Ascidiozooid of /'///•"-
soma, 640 ; in C'yathozooid of Pyrosoma,
634 ; in Salpa, 635 ; in X<-<i/<->ji<'n,/,;i. 282 ;
in larva of Si/iiapta digitata, 536 ; in
blastozooid of Urochorda, 638

Neural folds in embryo of Ami>]ii«.i-us
lanceolatus, 591 ; in Tornaria larva of
Balanoglossus, 578 ; in embryo of <'//ntIn'«
partita, 619

Neural groove, formation of, in Donacia, 258

Neural plate, formation of, iu embryo of
Amphioxus h/ncenlntug, 541 ; iu Tornaria
larva of l>iilan<>al<isss>ix, 578 ; in embryo
of Cynthia partita, 614

Neural tube, formation of, in embryo of
Amphio.cns lanceolatus, 593 ; in Toriiaria
larva of Balanoglossus, 578 ; in eniliryo
of Cynthia partita, 619 ; in embryo of
Salpa, 636

Neurenteric canal, formation of, in embryo
of .1 mphioxus lanceolatus, 592 ; in embryo
of Cynthia partita, 619

Neuroblasts ofD<»Ktci<i, 258 ; of ^\' '/>]i< 7 is, 161

Neuropore, formation of, in embryo of
Cynthia partita, 619 ; in larva of Am/i///-
otiix Imici-olatus, 593 ; in larva of Jiis-
tajilia, 632

Nitscliia, 506 ; cultures of, 131

Notochord, formation of, supposed in Actino-
trocha larva, 381, 383 ; in J mpli /<<.<•(/*, 592;
iu larva of C'l/iithin jiarfifa, 614; in New
England Tornaria, 579

Nuclear sap, definition of, 3

Nucleolus, definition of, 3

Nucleus of unripe ovum, 3

Nucula, 349

Nymphs of Hemimetabola, 287, 288

Oceania, 59 ; medusae of, 59
Ocelli of Dytiscus, 273, 274, 275
Octant of egg of Bertie, definition of, 91
Ocular plates of Kchinvs ewnli'nt nx, 577
Odonata, 245, 272, 277, 286 ; embryonic

development of, 266

Oesophagus, formation of, in Agelena, 235 ;
in Antedon r<n<acf«, 550; in Astficiis,
183 ; in larva of Asterias, 462; in larva
of Balanogloss/us clavigerus, 573 ; in larva
of Ophiotlu-i.i- f rag His, 4*7 ; in larva of
Synapta dif/itnln. 532 ; in T<'i-cln-ati<l!ii(i
septentrionalis, 411

Olfactory organ of Sni/iffn bipunctata, for-
mation of, 434

Oligochaeta, 128, 600 ; development of,
156-159

Ommatidium, formation of, in compound eye

of Axtneitx. 189 ; in compound cyt- of

l>iilisi-iia, 276 ; in lateral eyes of Limi'/nfi.

237

Onychophora, 169, 206, 285; development

of, 170-176

Oocyte of first order, 9 ; definition of. .",
Oocyte of second ordei-, 9
Oogenesis, definition of, 2
Oogonium, definition of, 3
Oostegites of Entoniscidae, '219
Oozooid of Botryllidae, 642 ; of Salpa, 640
Open larva of Patella, formation of, 307
Operculum of Patella, formation of, 303
Ophiopluteus larva, 498, 508, 509, 521,
529, 532, 533, 565, 654 ; compared with
Bipinnaria larva, 491, 492 ; compared with
Echinopluteiis larva, 51 1 ; definition of, 490
Ophi<>thri.,-j'r<i</ilix, 484, 501, 503, 504, 507,
508, 514, 529; abnormal development of,
502 ; development of, 485-498
<>jili //'/•«, larva of, 489
Ojihiura brereispina, 484 ; development of,

501-503

Ophiuroidea, 287, 461, 464, 456, 508,
514, 515, 522, 523, 530, 531, 534. 536,
538, 541, 542, 543, 560, 564, 565 ; de-
velopment of, 484-504

Opisthobranchiata, 280, 281, 291, 320, 321
Optic ganglion, formation of, in An/nfus, 184
Oral coelom, formation of, in Ant<'<l»i<

i-iixacea, 552

Oral cone of .1 iirHia, 69
Oral lobe of larva of Echinus esculenius, 509
Oral ring of plates, formation of, in larva of

Antedon rosacea, 547

Oral tentacles of T'wftw&m'a, development of, 56
Organ-forming substances, 658, 659 ; in egg
of Cynthia, 631 ; in egg of Dentalium,
330-332 ; in egg of Paludina, 309
Orgauogeny, definition of, 27
Orientation, methods of, 34
Orthoptera, 201, 245, 272, 277, 278, 286, -
Om-m-ella, 43, 44, 51 ; inet!imoriili»vi> of, 1 I
Osmic acid (Osmium tetroxide), definition of,

32 ; use of, 32

Ostium, formation of, in larva of Ani-i-/in, 71
Ostium of heart, development of, in Ai/c/cn'i.

229

Ostracoda, 177, 185 ; ancestral origin of, 212
n*i ,-i-a., brephic stage of, 22
n^hra Virginia no, veliger larva of, 348
Otocysts, formation of, in 1>> •iiliilium. •'!'_".' :
in Jtri'ixx'-i/xi'i. 342 ; in /.n/i;/". -'''^ : in
Paludina, 315; in Patella, 301; in
Xi/nii/iiii il'ujiliiin, 539

Ovary of Ascaris megalocephala, i:;> :
developmenl of, in .lulim. 2si •. ot
Miililiiln, 62S : of Phyllodromia, -<>'•'•
Oviduct, formation of, in Ascaris megalo-
cephala, 138 : in Molgula, 628, f,2(.i : in
Phyllodromia, 2ii3 ; inSagittabipimctata,
i:. i

( (viini (a) definition of, 11

684

IN VERTEBRA T A

Pachynema, definition of, 4
Pachytene threads, definition of, 4
Paguridae, 216

Paired tube-feet, formation of, in Asterias,
471 ; in Asterina gibbosa, 477 ; in Cucit-
i/inria p/itnci, 542; \\iEcliinusesculentiis,
517 ; (tentacles) in OphiothrLc fragilis,
495

PalatmoH, 192, 243

Pali, formation of, in Caryophyllia cyathus, 88
Palinurus, 214
I'nlltne, development of, 243
Pallial budding in Urochorda (Botryllidae),

637

Paludina, 319, 323, 335, 383, 415 ; de-
velopment of, 309-318
Pantopoda, 169, 285 ; development of, 242,

243

Paragaster of Sycandra raphanus, 43
Paragastric canals, formation of, in Beroe,

94 ; of Cteuophora, 561
Paraneuroptera, 245, 272, 277 ; embryonic

development of, 266
Parasyndesis, definition of, 4
Parenchyma, formation of, in Nephelis, 163 ;
definition of and formation of, in Plano-
cera, 168
Parenchyma-like tissue of larva of Berfie, 93,

95

Parthenogenetic ovuin(a), definition of, 2
Patella, 304, 310, 314, 317, 319, 321, 322,
323, 330, 332, 334, 335, 341, 375 ; de-
velopment of, 291-303
I'ufd/a. , -,,1'r/ilea, 291, 292
Patella rulgata, 291, 303
Pauropoda, 280, 281
Pea-plant, self- fertilized, 18
Pea-plants result of crossing, 1 6
Pecten, 348

Pectines of Scorpion, formation of, 241
Peetinibranchiata, 291
Pedal disc, formation of, in Urticina crassi-

cornis, 81

Pedal ganglia, formation of, in Dental ium,
329 ; in Dreissensia, 342 ; in Loligo, 358 ;
in Palndi.na, 315 ; in Patella, 301
Pedicellariae of Echinus esculentus, forma-
tion of, 515
J'edicel/itia, echinata, development of, 398-

403

Pedipalpi, 221, 241
Pelarjia, development of, 72, 73
Pelecypoda, 291. 463 ; ancestors of, 368,

369 ; development of, 332-353
Pelmatozoa, 456, 560, 564
Penaeidea, 177, 203, 208, 213
Penaeus, 655 ; Nauplius of, 22
Penetration path of spermatozoon in egg of

Cynthia partita, 611
/'in /in r/a, 61

Pentacrinoid larva of Anledon rosacea, 558
Pentacrinus, 558, 559
Pentacula, definition of, 539
Pentastomida, 221 242

Peracarida, 177, 219

Pericardial cavity, formation of, in Astacus,
187

Pericardial sac, formation of, in Chiton polii,
320 ; in embryo of Paludina, 311

Pericardial septum, formation of, in ])nnacia,
257 ; in Peripatus cape n sis, 174 ; in
Phyllodromia, 263 ; in Scorpion, 241

Pericardium, formation of, in dona in-
testinalis, 626 ; of Cyclas, 350 ; in Dnllcho-
glossus kou'alevskii, 583 ; in Dreissensia,
344 ; in Loligo, 362 ; in Paludina, 314 ;
in Peripatus capensis, 174 ; in Cyatho-
zooid of Pyrosoma, 634 ; in Scorpion, 241 ;
in New England Tornaria, 575 ; in Unio,
353

Perihaemal ring -canal, formation of, in
Oph tilth r LI- fragilis, 494

Perihaemal spaces, formation of, in Asterina
yibbosa, 474 ; in Opln'urn brcrispina, 502

Peri-oral coelom, formation of, in Asterias,
469 ; in Asterina gibbosa, 474 ; in Ophio-
thri.:1 fragilis, 497 ; in larva of Synapta
digitata, 536

Peripatus, 157, 187, 190, 204, 230, 232,
241, 244, 254, 257, 258, 261, 281, 283,
285, 287

Peripatus capensis, 167, 177, 657 ; develop-
ment of, 170-176

Peripatus novae-zelandiae, 226

Peripheral rosettes, formation of, in segment-
ing eggs of Gastropoda, 322 ; in seg-
menting eggs of Phascolosoma, 374

Periplasm of egg of Agelena, 222

Periproct, formation of, in Echinus esculentus,
518

Perisarc, formation of, in Tubularia, 57

Peristome, formation of, in shell of Acmaea,
304 ; in shell of Fissurella, 305 ; in shell
of HaUotis, 305

Periviseeral cavity, formation of, in Peri-
pi/tiis capensis, 174

Permanent anus, formation of, in Polygordius,
140, 142, 144

Perophnra, 638, 644

Per-radial lobe of stomach of Aurelia, 71

Phalliisi.t, 609, 631

riiiilliixin iiitiiiniiillata, 619

Pharynx, formation of, in Agelena, 235 ; in
Amphioxus lanceflatiis, 596 ; in larva of
< 'if nthia partita, 614; in larva of Doliolum,

637 ; in Cyathozooid of Pyrosoina, 634 ;
in Xalpa, 636; in blastozooid of Urochorda,

638 ; in Yungia, 114

l'l,<iscol<>*"nii/, 385 ; development of, 372-380

I'liiiM'iiliitinina gonldii, 373

Phascolosmna rnlgnre, 373

Pholas, 348

Phoronide'a, 372 ; development of, 380-385

Phoranis, 406, 560 ; development of, 380-

385

Phorozooids of Doliolum, 641
Phosphorescent organs, formation of, in Pyro-

soma, 632

INDEX

685

Phylaetolaemata, 385, 386, 396

Phyllocarida, 177

Phyllodromia, development of genital organs

of, 262, 263
Phyllopoda, 177. 185, 193, 211, 655 ; larval

history of, 200-201
Phyllosoma, larva of Loricata, 214
Physa, 291, 312, 320, 323, 338, 340
I'hi/.iiitia, 64

Pilidium larva, 118, 164 ; ancestral signific-
ance of, 127 ; development of, of Cere-

tii-Ktitlus lacteus, 120 ; metamorphosis of,

122-124 ; resulting from fragments of egg

and isolated blastomeres, 125
Pinnules of Antedoti rosaceu, formation of,

557
Piriform organ, formation of, in Cyphonautes

larva, 390
Pisidium, 349
Placenta, formation of, in embryo of Sal fin,

635

Plaice, 22

Plakiiia, development of, 44
J'lanocera, 161,332 ; development of, 103-112
/'fm/fn-bis, 322
Planula larva, definition of, 60 ; developed

from egg of free Medusa, 60 ; of Siphono-

phora, 65 ; compared to embryo of Cteno-

phora, 96 ; interpretation of, 98, 99
Platvctenea, 53
Platj helminthes, 118, 157, 161, 164, 320,

424, 600, 635, 661 ; development of, 102-

117 ; evolution of, 115-117
Pleopods, formation of, in Astacus, 188
Pleural ganglia, formation of, in Dreissensia,

342 ; in Lolir/o, 358 ; in Paludina, 315
Pleuron, formation of, in Linn/lux, 238
Pleuronectes, 22
Plexus of muscles in larva of

appendicvdatus, 148
Ploima, 418
Pluteus paradoj'iis, 489
Podarke, 129
Podaxonia, 406, 407, 415, 416; development

of, 372-385
I'oilocoryne, 72 ; development of Medusa of,

61

Poison-gland, formation of, in Ayelena, 235
Polar bodies, homologies of, 13
Polar lobe in egg of /fentalium, first, 326 ;

second, 326 ; third. 327 ; in the egg of Ilij-

niKissa, 332
Polian vesicle, formation of, in Si/n<i/,tn

d/i/itata, 538
Polychaeta, 128, 161, 205, 211, 285, 372;

development of, 153-156
Polyclada, 102, 117, 164 ; development of,

103-115
Polygonlius, 106, 153, 154, 155, 156, 158,

161, 163, 164, 165, 166, 293. 294, 299,

301, 305, 306, 310, 321, 323, 324, 335,

343, 387, 388 ; development of, 128-153
Polygordius appendiculatus, 152 ; later

larval development of, 144-152

s lacteus, 144 ; metamorphosis of,

152 ; later larval development of, 151, 152
Polypliinii/x, 193
Polypide in Polyzoa, 644 ; formation of,

in Cyphonautes larva, 394 ; in Polyzoa

Ectoprocta, 396
Polyplacophora, 291
Polytrochal larva, definition of, 153 ; of

Nereis, 156

Polyzoa, 560, 562, 569, 608, 644, 655 ; de-
velopment of, 386-403
Polyzoa Ectoprocta, 372, 386, 403, 405, 40H,

656 ; development of, 387-396
Polyzoa Entoprocta, 385, 386, 564, 622 ; de-
velopment of, 398-406
Pomatoceros, 129, 130, 131, 155
J'i',if"j>/i/7tis, Mysis larva of, 215
Porania pulwillus, 472
Pore-canal,. formation of, in larva of Axtcrin*.

465 ; in larva of Oji/iivt/i /•/> f'l-ni/i/is, 489 ;

in Opliiiirn lii'i'i-iKjiiiiii, 501
Pores of shell ofTt'r<'//i'i//n/i/iasepteiit/'ionalis,

413
Porifera, 116, 660 ; compared with Coelen-

terata, 53 ; development of, 37-52
Porocyte, ancestral meaning of, 52
Porocytes of Grantia, 43
Portuuion, development of, 219, 220 ; young

and adult stages of contrasted, 22
Posterior amniotic fold in embryo of h«n<n-i« ,

249 ; in embryo of IJoryphum, 261 ; in

embryo of Odonata, 266
Posterior ciliated epaulettes, formation of,

in larva of Ecliinmt fxculentus, 515
Posterior endodermic thickening, formation

of, in embryo of Iinm/riii, 253
Posterior funnel fold in embryo of I.nlii/n,

357
Posterior mantle -groove of 7V/v///v////////if

septciiti-l'itinlis, 410

Posterior mesenchyme. formation of, in em-
bryo of CyntJ/in /i/i rt if a, 615
Posterior mesoderm, formation of. in embi-yo

of Axi'urix i/ii'i/tduci'/ilitda, 445
Posterior sinus, formation of, in /,< •//</'•, '•'•>>-
Posterior vacuolated crest in hirva of <>ji//in-

thri.i- /1-i.njHix, 488
Postero-dorsal arms of cili;ited bund in larva

of Axtrrinx, 465: in larva of

esci//i'/iti(x, 509; of larva of

fragilis, 4!'0 ; of larva of ,sv/»v^" <li<i!t,it<i,

'533
Postero-dorsal rods in larva of l-sliimtx

esculent a*. 509
]'M>tero-lateral arms of ciliated bund of larva

of Axt'-riii*. lii.'i; of larv:i of Echinocardium

cordatum, TiL'-J : of l.-n-va of Ophiothrix

fri/<iilix, 487; of larva of Synapta ihj/itn/it,

.",:;:', : of New Hn-lan.l Tornaria, 57('>
Post ero- lateral i",!-, in larva of i//,/,,',,.'

fi-ii'tilis, 487
Post-larval (h^vdopment of Asteriiut .///,/....-.'.

17'.'. 180; of Echinus esculentua, 520. 521
Post-oral arm of Pacific Tornaria 581

686

INVERTEBRATA

Post-oral arms in larva of Asterias, 465 ; of
larva of Mi in us esculentus, 508 ; of larva
of o/iliiiitliri.'- j'rinjHis, 490 ; of larva of
Syniijiln ilii/iiiitii, 533

Post-oral band of cilia in larva of Asteriax,
464

Post-retinal layer, formation of, in central
eyes of A'/i'/cnn, 234

Prae-oral arms of ciliated band in larva of
Asterias, 464 ; in larva of Echinus escu-
lentus, 509 ; in larva of Synapta <li<tit«la,
533 ; in New England Tornaria, 576

Prae-oral band of cilia in larva of Asterinx.
464 ; in larva of Phascolosoma, 376

Prae-oral coelom of Actinotrocha larva,
381

Prae-oral lobe, disappearance of. in Actino-
trocha larva, 383 ; of larva of Asterinc
gili/iuMi, 473

Prae-oral loop of ciliated baud in larva of
Asferias, 464 ; in larva of >'///«'///«
il it/ Hutu, 532 ; of New England Tornan;i,
576

Pre-anal spine of Nanplius larva of Cirripedia,
202

Pre-autennae of Scolopendra, 282

Premandibnlar cavities of Vertebrata, 606

Preservation of eggs, methods of, for Amplii-
u.i-ns l/i iiceoli/l UK, 587; for Antedon rosacea,
545: for Asmr/* n/i'i/n/ucephala, 438, 439-;
for Astacus, 178, 179 ; and larvae for
Astcruiili-a, 458, 459, 460; for Aurelia
aurita, 67 ; for Cynthia partita, 609 ; for
Donacia, 245 ; for Ltreissensia, 333 ; for
Firin/i, 320 ; and embryos and larvae for
Grant ia, 38; for Pa fell a, 292; for Phi/*u,
320 ; for Polygordius, 129, 130 ; for
Sin/ Hlii, 428 ; for Urticina i-r<_i^sii-i,r,iix, 76

Priapuloidea, 163, 372

Primary body- cavity, 165; of > larva of
Anti'rias, 461

Primary cerebral ganglion of Astacus, 184

Primary dorsal organ, formation of, in em-
bryo Of hiniiii-iii, 247

Primary germ-cells, formation of, in Phyllu-

tf nun in, 262
Primary germinal involution of Asterinn

i/iMiosa, 481
Primary gill-slits, formation of, in larva of

A'nijihiu.i-iix lanceolatus, 590
Primary niadreporie pore, formation of, in

embryo of Anfcifnn rosacea., 547 ; in larva

of Axli-riii ft, 465 ; in larva of Ophiuthr/.''

fragilis, 489
Primary mesenchyme, formation of, in larva

of Echinus esculentus, 507 ; in Ophintli.ri.i-

fragilis, 486
Primary mesoderm, formation of, in Astacus,

181
Primary radial plates, formation of, in

A ii/i'ilnii riisdi-i'd, 556
Primary stomodaeum, formation of, in

( 'nil ill i mi i nsseola, 422, 423
Primary tmchoblasts, formation of, in CV<y</-

dula, 321 ; in Fiona, 321 ; in

295 ; in Phascolosoma, 374
Primary yolk pyramids of egg of Astern*.

180 ; of eggs of Scolop* ndra, I'sl
Primitive anus, formation of, in 7W////I. /•<////.>•.

139
Primitive cumulus, formation of, in embryos

of Arjdcna, 224 ; in embryos of Donacia,

247 ; in embryos of Pedipalpi, 241 ; in

embryos of Scorpion, 240
Primitive germ-cells, definition of, 2
Primitive mouth, formation of, in 7V///-

ijunUus, 139
Primitive streak in eggs of Cephalopoda, 356 ;

in embryo of Agelena, 223 ; in embryos

of Pedipalpi, 241 ; in embryos of Pcri-

patus capensis, 171 ; in embryos of

Scolopendra, 282
Principal retractor muscles of Trochophmv

larva of Phascolosoma, 376
Proboscis, formation of, in CallliUitu ri/ssen/n,

424 ; in Nemertinea, 123 ; in New England

Tornaria, 577
Proboscis cavity, formation of, in Bulnni,-

ylossus clariijfriis, 571
Proboscis pore, formation of, in Bal'anoglossus

clavigerus, 572
Proboscis sheath, formation of, in Nemertinea,

123
Proctodaeum, formation of, in Aiji-lrmi, 226,

231 ; in Astacus, 183 ; in Bombyn, 280 ;

in Callidina russeola, 425 ; in Jtnnai-in.

253, 254 ; in D-reissensia, 337 ; of larva

of (ftilt'i -11,-i'lln nlnti, 269 ; in Cyphonautes

larva of Mcml/ranipora, 390 ; in Pcrfid-llim/

i <-l/i in/tit, 400; m Peripatus capensis, 175
Progoneata, 280, 281, 285
Pronephros, 162
Prosobranchiata, 291, 320, 324
Protandrons, definition of, 2
Protista, 660
Proto-annelida, 416
Protobranchiata, 349
Protocephalic region of embryo of Dmiaciu,

251
Protocerebrum of Astacus, 184 ; of ]>oiu«-i</,

258 ; of Scoloptndm, 283
Protochordata, 381 ; development of, 568-

648

Protocoelomata, 436 ; denned, 661
Protocormic region of embryo of lionacin,

251

Protogynons, definition of, 2
Protonemertinea, 118
Protonephridium of Echiuroidea, 163 ; of

l'<iliiiii,r<liits, 145 ; of Polygon I i ii. * «/>/>i-i/-

diculatus, fate of, 150 ; of Polyy<>r<H<"<

lacteus, fate of, 152
Protostigmata, formation of, in f'i«n<t intesti

•nafis, 627 ; in larva of Doliolmn, 637
Prototracheata, 169, 170
Prototroch, of Polifyonfins upjwwliriiltihi*,

destruction of, 150 ; disappearance of, in

larva of 1'hascolosoma, 377, 378 ; forma-

INDEX

087

tion of, in Annelida, 321 ; in

/'ictens, 120 ; iu Detitaliiiin, 328 ; in Ltrcis-

.11- a. -«'it, 337 ; in ailult Entoprocta, 386 ; in

Echiuroidea, 163 ; in Palttdiiiu, 310 ; iu

PuteRa, 293, 29? ; in Pdyyonlim, 134 ;

in Xijiintcttlits, 380
Protozoa, 20, 30
1'rotozoaea larva of EitpJiaitsiit, 203 ; of

Penaeus, 203
Pseudozoaea stage in development of Stomato-

poda, 218

Pulmonata, 291. 320
Pupa of Cirripedia, 202 ; of D'ntccic, 260 ;

of Gah'i'iicella itli/ii, 268 ; of Holothuroidea,

585 : of Siiri-i/tiitti, 202 ; of Si/ituj/fi/

t/iffitc.ta, 538
Pupal phase of development, definition of,

28 ; interpretation of, 656
Pui-punt, 320
Pyloric caeca, formation of, iu A*ti.'rii/*,

•171 ; iu Afttt.-riiiii ijililmmi, 477
Pyloric gland, formation of, in Cimia. in-

testinalis, 625

Pyloric sac, formation of, in Asterias, 471
Pyrosoma,637, 639 ; development of, 632-635

Quadrant of egg, definition of, 106
Quartettes of micromeres, definition of, 106 ;
formation of, in segmenting egg of Pat<-Iln,
293-295 ; in segmenting egg of Planocera,
106 : in segmenting egg of Polyyonlius,
133-139

Radial canals of medusa of TV />/'/'' /'/f, 58
Radial cells in embryo of Polygordius, 135
Radial nerve-cords, formation of, in <>ji/iin-

thri.<:frarjiUs, 498
Radial perihaemal canals, formation of, in

Asteriiia gibbosa, 475 ; in Echinus escu-

lentus, 515 ; in Ojihii.it/iri'- f'mi/i/is, 494,

495
Radial plates, formation of, in Ainji/iinrn

sfjiKimi.tta, 499 ; in A.ifi'rinn i/ihtiiisa, 479
Radial shields, formation of, in Ai/tji/ii/'rit

fH/iitiiiititii, 499

Radial water - vascular canals, formation of,
in Antedon i-osucr-c, 549, 556 ; in Ast'-rii'.*,
471 ; iu f.'ii.ciiiiKirin planci, 542; in Ophio-
lltri.i: fi-agilis, 492 ; in St/ii<ij>f</ i/ii/i/ufi/,
533, 539

Radiating muscles, formation of, in J'ol;/-
i/in-t/ii/n iipj>t-iit./i'-n/iitii.i. 150

Radius of embryo of Pa/i/i/un/ius, 135

Radula-sac, formation of, in Loligo, 358,
363 ; in PaluiUiKi, 315 ; in I'ntell,', 301

Rat, development of spermatozoa of, 7

Rathken, medusa of, 59

Recapitulation theory of development, 20-
25, 649 ; presuppositions of, 220

Rectum, formation of, in Asteri"*, 171 ; in
Asterina yibbosa, 478 ; in embryo of
Pedicettina, 400

Recurrent coil of intestine, formation of, in
csculentus, 520

Reducing division, detinition of, ii
Regeneration of eye in Shrimps, 286
Jt'-iiift" renifornis, ili-vi-lippmunt of, 87 ;

formation of skeleton of, 88
Reno - pericardia! canal, formation of, in

Dreissensia, 346 ; in l.«H<j«, :i62 ; in

Paludittn, 314
Retinula of compound eye, formation of, in

Astacus,189; inDytiscus,27Q', iu Lin

237
Retraction of polar-lobe in egg

326
Retractor muscles of foot, formation of, in

itivi.-i.-ii-ii.iiti, 342 ; of funnel, in /,«//</.»,

361 ; in lars-a of /V//.</c;-i////\ appendicu-

fn/iis, 148

, process of, in develoj)inent of
, 227 ; in development of Jin, /</,•;./,

259 ; in development of /'i-riji/iim-fn, 260
Rhabdites of Ynm/iii, 115
l.'habditis larva of Am-'/ri.i //(-y/'"'"'t'1/'/"'/",

447 ; of Nematoda, 454
Rhabdocoela, 102, 115
Rhabdocodida, 102
Rhabdome, formation of, iu eye of Affcfem/,

233, 234 ; in compound eye of Ax/m-nti,

189 ; in compound eye of Dytiscus, 276
Rhagon of Oscurella, 44
Jt/ti:m:ri/ti(.i, 559, 560
Rhyncobdellidae, 128, 161, 284
Ribs of Bertie, formation of. 92
Right anterior coelom of larva of Aster i <s

467 ; of larva of />///, //<\ esculenttis, ">09 ;
of larva of Ophiothrix fragilis, 490

Right hydrocoele, development of, in larva
of Asterias, 466 ; in larva of Asterinn
ififi, 474; in larvae of Echinus escu-
and Echinn.1 miJiiiris, 528; in
larva of Ophiothrix fragilis, 491
Right madreporic pore in larva of Axtrritix,

465

Right posterior coelom of embryo of A ntedon
rosacen, 547 ; of larva of Asterias, -l'!7,

468 ; of larva of Eclii/tn.i esculentus, 509 ;
of larva of «/;///«////•/.<• r',-n</i!i.i, 490

Right ventral horn of left posterior coelom
in larva of Axtrriiis, 468; in larva of
Axt'-i -iiin i/i/ifnisii, 471 ; in larva of 7v7/ ////'.•>•
esculentus, 514 ; in larva of i>/,/n'n///ri.'-
fragilis, 494

Ring muscles of larva of I'lJiii/m-dins <tfi-
pendiculatus, 148

Ring-sinus, formation of, of larva of . I /'< •«//".

71

i;i]»- ovum, definition of, 9

Rosette-cells in embryo of l'<itrlln, 'J'.1 1 :

formation of, in embryo of

133
Rosette plat'1, formation of.

rosacea, 558

l;.i-li-al spine of Ax/urns, 189; of'Proto/oa.a

larva of Penaeiis, 203
Kotiu-ra, development of, 418-427
Rnfrle of spermatozoon, definition of. 7

688

INVERTEBRATA

Sabelliformia, 128, 154

tfabineu, MysLs larva of, 215

Sacculi, formation of, in Antedon rosacea, 552

Kdi/drtid /inrdxitii-it, 85

Sagitta bipnnctata, development of, 428-435

Salamander, changes induced in by changes

in environment, 651
Salivary glands, formation of, in Callidina.

russeola, 424 ; in Loligo, 358, 364 ; in

Peripattis capensis, 175
tialpa, 637, 639, 640 ; development of, 635,

636
Scaphopocla, 291 ; ancestors of, 368, 369 ;

development of, 325-329
Scarabaeidae, 277
Schizocoele, formation of, in Pobjyurtlitm

appendiculatus, 150
Schizopoda, 177, 185, 192, 202, 210, 213,

216, 218
Seirtopoda, 418
Scleroblasts of Grantia, 43
Scoleciformia, 128, 153

Kcolopendra, 285 ; development of, 281-284
Scorpion, 221 ; development of, 239-241
Scorpionidea, 221

Scutum, formation of, in Cirripedia, 202
Si-i/llnriix, 214

Scyphistoma, 72, 75 ; of Aurelia, 70
Scyphozoa, 78, 79, 96, 166, 661 ; develop-
ment of, 67-76

Sea-anemone, definition of, 87
Sea- spiders, 242
Sea-urchin, eggs of cross - fertilized with

foreign sperm, 17
Second maxilla in Astacns, 186
Second maxillary segment in Donacia, 252
Second polar body, definition of, 9
Second somatoblast in segmenting egg of

Dreissensia, 335 ; in segmenting of JYereis,

156
Secondary body-cavity, equivalent to coelom,

165
Secondary dorsal organ, formation of, in

Donacia, 247, 259
Secondary germ - cells, formation of, in

Donacia, 263
Secondary gill-slits, formation of, in larva of

Amphioxus lanceolatus, 604
Secondary madreporite, formation of, in

Si/iiapta digitata, 539
Secondary mesenchyme, formation of, in

Ophiothrix fragttis, 487
Secondary mesoderm, formation of, in egg of

Astacns, 181
Secondary radial plates, formation of, in

Antedon rosacea, 556
Secondary stomodaeum, formation of, of

Callidina russeola, 423
Secondary stone - canals, formation of, in

Antedon rosacea, 557
Secondary trochoblasts, formation of, in

embryo of Crepidula, 321 ; in embryo of

Fiona, 321 ; in embryo of Patella, 297 ;

in embryo of Phascolosoma, 375

Secondary yolk pyramids, formation of, in
egg of Astacus, 183

Segmentation-cavity, 165

Segmentation of coelom of Asteriitu
472, 473

Segmentation of the egg, definition of, 27

Segmentation of the egg of Agelenu, 223 ;
of Amphioxus lanceolatus, 586, 587, 588 ;
of Antedon rosacea, 545 ; of Ascni-i*
megalocephala, 440-443 ; of Astacits, 179,
180 ; of Asterias, 460 ; of Aurelia <//> /•/'/»,
68 ; of Balanoglossus daviyerus, 570 ; of
Beroe, 89-92; of Branch iptis, 194; of
Callidina russeola, 419-421 ; of C'ere-
brat.nl us lacteus, 119 ; of Cucumaria pland,
541 ; of Cynthia partita, 612-614 ; of
Dentalium, 326-328 ; of Loliclwylossus
pusil/ifs, 583 ; of Donacia and of Itori/-
phora, 246 ; of Dreissensia, 333-338 ; of
Echinus escnlentus, 506, 507 ; of Mu-
p/ianxia, 192 ; of Geryonidae, 67 ; of
Holothnria tubitlosa, 541 ; of Juius, 284 ;
of List's, 195 ; of Macrobwtus, 243 ; of
Membmnipora, 387 ; of Neiihelis, 160 ;
of <>pl, /',,f /i ,-/'.>• frai/ilis, 486 ; of 1'allene,
243 : of Paludina, 310 ; of Patella, 292-
295 ; of PediceUina, 398 ; of Penpa/nx
capensis, 170 ; of Phascolosoma, 373-375 ;
of Planocera inqnilina, 104-109; of
Polygordius, 131-139 ; of Polyplienin.-i.
193 ; of Pyrosoma, 632 ; of Sagittn
/>;/nmctata, 428, 429 ; of Salpa, 635 ; of
Scolopendra, 281 ; of the Scorpion, 239 ; of
Sepia, 354 ; of Sycandra raphnnus, 37,
38 ; of Synapta digitata, 530 ; of Tere-
/intti/Iiiia septentriiiiinlix, 408 ; of Ti'lm-
laria mese'inbryanthemmn, 54 ; of Urticina
crassicornis, 77

Segmentation of mesoderm, cause of, in
Annelida, 165

Segments, formation of, in embryo of
A ijelena, 225

Sense-tentacle, formation of, in A urelia. 72

Sensory-plate of larva of Asterias, 461

Sepui ojliri/Kilis, 353, 354, 366

Septa, formation of, in Can/npln/Ui/i I'l/nf/i/is.
87

Septal funnels, formation of, in larva of
Ai'.'dia, 70

Serosa, formation of, in embryo of Do)it.«:!<i,
247 ; in embryo of iJuri/plmri/, 261 ; in
embryo of Lepisma, 265 ; in embryo of
Modules, 265 ; in embryo of the Scorpion,
240

Serpulidae, 416, 520

Ki'rtnlni-io, development of gonophore bud of,
62

Sex-chromosomes, 13, 15

Sexual germ, definition of, 2

Shell, formation of, in Acmaea, 304 ; in
Dentalium, 329 ; in Dreissensia, 339 ; in
Fissure/la, 305 ; in Haliotis, 305 ; in

357

in Cyphonautes larva of
, 392 ; in Ifautilis, 357 ;

INDEX

US'.)

iii Patella, 300 ; in Sepia, 357 ; m 7V,v-
brati'li/iii fii'iiti'iitrinuiilis, 413

Shell-gland, formation of, in (_'i/cloj>s, 199 ;
in larva of Denti/Uinn, 329 ; in larva of
Jhrififciixiii, 335 ; in embryo of L"li(/<>,
357 ; in larva of Patella, 299

Siphonoglyphe, definition of, 83

Siphonophora, 53, 161 ; development of,
64-66

Sipnnculoidea, 163, 372, 406

Sipit-ncultis, 385 ; development of, 380

Slime glands, formation of, in Perlpatus
1-ii/nnsis, 175

Solaster, 459, 481, 484, 501, 565, 656

Solaxti'i- fiiileca, 457, 529 ; development of,
482

Solenocytes of archinepliridium of Poh/-
gordins, 140; of larval kidneys of Gastro-
poda, 323 ; of nephridia of Aiiipliiu.i'iix
li/iiceolatus, 600 ; of nephridium in Polij-
gordius, 138

Solenogastres, 291 ; ancestor of, 368 ; de-
velopment of, 324-325

Somites, definition of, in Polygordius, 145 ;
formation of, in embryo of AMjihiu.viix
In iie<'i>lat us, 594 ; in embryo of Astact'*.
187 ; in embryo of Don aria, 251 ; in
embryo of Pei-iimtus enpensis, 171

!<l>n, Idla, 428

S<l>iii?ella draco, 433

Spadix of medusa of Titbularia, 58

Spatangoidea, 511, 565

Spermatic!, definition of, 6

Spermatocyte of first order, 6 ; definition of,
3 ; of second order, definition of, 6

Spermatogeuesis, definition of, 2

Spermatogonium, definition of, 3

Spermatozoon, definition of, 2 ; formation
of, 6, 7

Xji/idem'/iinns, 525, 526

Xji/it/ei-ec/iinits graiii'/cris, 504

Sphaeridia, formation of, in Ei-lii/nm escu-
li.'ittt/s, 520

Xt>;<ters, 282

Spinal cord, formation of. in AmpMoxus
lanceolatus, 593 ; in larva of Cynthia
partita, 619

Spines, formation of, in llrhiniis fxi-nlentus,
515

Spinnerets, formation of, in Af/rlaut, 231

Spinning glands, formation of, in Agc/ena,
231

Spiouiformia, 128

Spiral caecum, formation of, in Loligo, 365

Spiral cleavage of egg of (.'erebi-dtnlns lacteus,
119 ; of egg of Dreissensia, 333-335 ; of
egg of Patella, 293-295 ; of egg of P1,ns-
I'lilii/na, 373-374 ; of egg of J'lanueera,
104-108; of egg of Polygm-dius, 129-139

Spiral twisting of Polu<ii/i«, distinguished
from torsion, 316-317

Splanchnocoele, formation of, in J mpli inrns
lanceolatus, 595

, development of. 47

rix, 50

Squame of antenna in Zoaea larva of
Caridea, 210

Stalk, formation of, in larva of Antedow
rosacea, 548 ; in larva of Asterlii*, Jii'i ;
in larva of Petfi<r//i,i,<. JO-'! ; in larva of
Terebi-nt ul !na, 412

Star-fish, *perm of, used to cross ft-nili/,-
eggs of Sea-urchin, 17

Stercoral pocket, formation of, in Afieli-im
230

Htei-HHspix, 153

Sti-riiuni, development of, of >•'<•<•/«;»'/, «/,-,.
282

Stigmata, formation of, in L'ionn intextimili.-i,
628 ; in Itonatia, 258, 259

Stolon, foi'ination of, in Diplosomidae, (i4i! ;
in Liolinlinii, 639 ; in Pyrosoma, 639 ; in
Salpa, 639 ; in Urochorda, 638

Stolouial liuddiug in Urochorda, 638-641

Stomach, formation of, in J//</o/", 235 ; in
adult Asterias, 469, 471 ; in larva <>\
Asterias, 462 ; in larva of Il< ila/n n/ln** us
clavigerus, 573 ; in (.'iumi lut^tinuli^,
625 ; in Dental I urn, 32S ; in L<>l/</i>. :',t)4 :
in Cyphonautes larva of Mfiiiln-niiijinrii.
389 ; in larva of Ophiothrix fragilis, 487 ;
in larva of I'l-dn-cUi nn, 400 ; in larva of
Polii<in,->i;nx, 142 ; in larva of >'////"/</"
ifii/itata, 532

Stomatopoda, 177, 219 ; development uf,
216-218

Stomocot'lc of AnijiJi iu.i-iiH In i//-i'i>liil us, 006

Stomodaeum, definition of, 76 ; formation
of, in Ai/i'!<_'iia, 226 ; in Amphi».i-i<fi lanceo-
latus, 604; in embryo of Anteili'n rosacea,
547 ; in A scar is megalocephala, 444 ; in
Astaciis, 183, 184 ; in larva of Axfri-id.'..
462 ; in larva of Balanoglossus clavigerus,
573 ; in Beroe, 94 ; in /.'«////<//.•, 279 ; in
Crepii!n/<i, 323; in Hrva of Cucumaria
ji/aufi, 542 ; in Jh'nfulinin, 328 : in
liiiinifiii, 252, 253 ; in Ih-eissviisiu, 336 ;
in adult Echini's esculentus, 515; in
larva of Eclnnns i-xmli-iit UN, 508 ; in
Fiona, 323 ; in Cyphonautes larva of
Ale'iiilii-iiiii/nn-n, 389; in ..V. •////(//*, 160;
in larva of Opkiothrix fragilis, -1S7 : in
Paludina, 310; in Patella, 2^ ; in I',-<li-
i-i-lliua, 400; in l'< '1-lpntnx <;/ji, -;/,v/x. 17.">;
in J'lifixi-nl, ixuiiiii. :;7<i : in /'////>•». 32 1 ; in
PlaiK'i-i-i-ii. 109; in /'"///'/'</.///'-. 137-138,
323 ; in >«<////,/ bipunctata, 131 ; in l,-ir\;
of ^i/nii/ifd <i;<iitnfii, 532 ; in Trnl.nif,,/!,!,!
septentrionalis, 110; in l'ni«, M52 ; in
Urticina crassiwrnis, 7'.' ; iiii'taiimrpli
(it, in larva uf (inUi-i-n,-i-l/i nhni, 269

x/<i,iiiitiii;i apicata, di^i-lupmcnt of, 61

Stonr-c:iii;il t'lii-iiiatioii of, in Antedon rosai
550; in .l.v/ivi'i/*, 469: in AxfiTinii </</,/»
474 ; in AV7//////.S- . scvlentus, 51 u : of '//,/,/,,.
flii-i.'-fi-iiijilix, 491 ; in ttjdniirii /-/•- vispina,
501 : in Xiiii«/it<t iiiijitiitu, 533

stiv|^in,-nia, definition of, I

690

INVERTEBRATA

Strepsitene thread, tlefinition of, 4
Strobila of .1 mrtin, 72
Stabilization, 75 ; definition of, 7'2
Strongylocentrotus, 511, 630; egg of, 3;

eutelechy of, 21

Strongylocentrotus droebachiensis, 505
Strongylocentrotus franciscanus, 505
Strongylocentrotus lindus, 504, 506
Strongylocentrotus pnrpi'mtus, 505
Sub-genital pit, formation of, in Aurelia,

71
Sub - intestinal ganglion, formation of, in

Paludina, 315
Sub-neural gland, formation of, in Ciona

intestinalis, 625 ; in blastozooid of Uro-

chorda, 639
Sub-neural sinus, formation of, in Peripatus

capensis, 174
Sub-oesopliageal ganglion, formation of, in

Ag>:/i-iin. 232, 235 ; in the Scorpion, 241 ;

in Teri-liratiilinit x<-/i/t-iit,-i<->iinlit;, 412
Sub-stomachal canals, formation of, of Beriie

94
Suli-tentacular canals, formation of, in Jie,;',, ,

94
Sucker (internal sac), formation of, in Cypho-

nautes larva, 392

Sucker muscles of Cyphonautes larva, 393
Sucker of Cyphonautes larva, 401, 406 ;

e version of, 394
Sucking tube, formation of, in Achthcres am-

bloplitis, 207
Supporting lamella of Urticiiia crassicurnix,

79
Supra-intestinal ganglion, formation of, in

Paludina, 315
Supra-oesophageal ganglion, formation of.

in Siii/itin h!i>niicta-ta, 432 ; in Tere-

bmtulina sepfe/ifrimiaUs, 411
S)/candrn raphanus, later development of,

43 ; segmentation of the egg of, 35
Syconidae, 37
Symmetrical post-larval stage of Anomura,

216

Symphyla, 280, 281
S//nnpt/i, 547, 565

Synapfn </////////<>, development of, 529-541
^i/iiapta vivipam, 529 ; development of,

539-541
Syncarida, 177
Syndesis, definition of, 4
Synizesis, definition of, 4

Tactile organ of Sagitta bi^inii'tntn, 433
Tadpole of Ascidians (Tuuicata), 654 ; of

simple Ascidiau, 619-622
Tadpoles, determination of sex of, 17
Taemolae of larva of Aurelia, 69 ; of Beroe,

94 ; of medusa of Tubular ia, 58
Tail, formation of, in larva of Ainptu'<i.>-iix

in nceolatus, 596 ; in CaUidina ri'ssco/n.

423 ; in embryo of Cynthia partita, 618 ;

of Spermatozoon, definition of, 7 ; of l.irv;i

of Tuuicata (Urochorda), 608

Tail-bud, formation of, in larva of Amphioxus

lancculatUK, 596
Tail-eudoderm, origin of, of larva of Cynthia

partita, 614

Tardigrada, 169 ; development of, 243
Teeth, formation of, in Echinus esculentus,

515

Teleostei, 22

Telescoped development, definition of, 153
Teloblast of Oriodrilus lucuum, 158 ; of

Nephelis, 161 ; of Poh/unr/Iius, 144
Telolecithal egg, definition of, 26 ; of Cepha-
lopoda, 354 ; of Scorpion, 239 ; of Peri-
jiKti's, 177

Telotroch of Tornaria larva of .Brtfr/;/n//A«x//.v
clavigerus, 574 ; formation of, of larva of
Dreissensia, 337 ; in larva of Patella, 299 ;
in Actinotrocha larva of Phoronis, 381 ;
in larva of Polygordius, 140, 144
Telotrochal larva, definition of, 153
Telson, formation of, in Astacus, 189
Tendon-cells, metamorphosis of, in larva of

Galcnicella id mi, 208
Tentacle pockets, formation of, in CaUinnira,

95
Tentacle-sheath of Bur/nla, development of,

in bud, 397

Tentacles, formation of, in Antedon rosacea,
550, 551 ; in Callianira. 95 ; in Paludina,
315 ; in Pedicellina echinata, 403 ; in
Phascolosoma, 379 ; in Actinotrocha larva
of Phoronis, 381 ; in adult Phoronis, 383 ;
in Polygordius appendiculatus, 148 ; in
medusa of Tubularia, 58
Terebellidae, 157
Terebelliformia, 128, 153
Terebratidina septi n/,-i,,,i<>lis, development

of, 407-413
Teredo, 348
Terguni, formation of, in Cirripedia, 202 ;

in Li mains, 238 ; in Scolopendra, 283
Terminal jihites, formation of, in Amplii urn
squamata, 499 ; in Asterina gibbosa, 478 ;
in Echinus esculentus, 517
Terminal threads of ovaries, formation of, in

Phyllodromia, 263

Tertiary radial plates, formation of, in Ante-
don rosacea, 556

Test, formation of, in simple Ascidian, 622
Test-cells in larva of simple Ascidian, 622
"Test-cells " (follicle cells), in egg of (.'i/nthia
partita, 610; of Pyrosoma, 632; of Salpa,
635

Testicardines, 406, 407

Testis of A scar is megalocephala, 438 ; forma-
tion of, of Molgula, 628
Tetrads, definition of, 12
T-giants, development of, of Ascaris mcgalo-

cephala, 448, 449
Thalassinidae, 215
Thaliaceae, 568, 608, 635, 636, 637
Thaumatocrinus, 560

Theca, formation of, in Caryophyllia cyaihus,
87

INDEX

691

Thecidium mediterraneiim, 407

Thecoida, 456

Thoracic region of embryo of Donacia, 251

Thoracico-abdominal rudimeiit in embryo of
Astacus, ISO

Thysanura, 245, 287, 288

Tiara, medusa of, 59

Tip-cells of Molluscan cross in embryo of
Crepidula and Fiona, 321, 322 ; in em-
bryo of Patella, 294, 297

Tipulidae, 278

Tongue -bars, formation of, in Amphioxns
fmiceoliitiis, 604 ; in New England Tor-
uaria, 579

Tornaria, 1, 569, 582, 585, 605, 606 ; of
Jii//n, /, i:///is.^i/\ d<n-i<ji'rns, 574 ; develop-
ment of, of Nassau, 579-581 ; New Eng-
land, 574-579; of Pacific Coast, 581,
582 ; interpretation of, 661

Torsion of larva of A cmaea, 304 ; of embryo
of Paludina, 315, 316 ; of larva of Patella.
300

Tracheae, formation of, in Agelcna, 231 ; in
Donacia, 258 ; in wings of Doryphora, 273 ;
iu Peripatus capensis, 175

Tracheoles in wings of Doryphora, 273

Trachymedusae, 53 ; development of, 67

Transverse ciliated rings, formation of, in
larva of Antedon rosacea, 546 ; in larva of
Cucumaria planci, 542 ; in larva of
Synapta digitata, 536, 537

Transverse commissures, formation of, in
nervous system of Astacus, 185

Trematoda, 102, 103

Triaxouia, 37

Triclada, 102, 103

Trilobita, 169, 205, 238, 244, 285, 286

Trilobite larva of Limnlus, 238

Tritocerebrum of Astacus, 184 ; of Donacia,
258 ; of Scolopendra, 283

Trochal disc, formation of, in Callulina rus-
seola, 424

Trochophore larva, 390, 405, 406, 408, 411,
415. 416, 427, 561, 655, 661 ; interpreta-
tion of, 164 ; of Acmaea, 320 ; of Annelida,
description of, 130, 368 ; of Annelida,
compared to Nauplius, 204 ; of Dental i inn,
328 ; of Dondersia, 325 ; of Dreissensin,
337, 338, 368 ; of Eupomatus, 154 ; of
Fissurella, 320 ; of Haliotis, 320 ; of
Paludina, 310 ; of Patella, 298, 368 ;
of Phascolosoma, 370 ; of Polygordius,
139 ; of Polyplaeophora, 320 ; of Sipuncu-
loida, 163, 372 ; of Trochus, 320
Trochus, 320, 322, 323

Trophi, formation of, iu C«llidinn russeola,
424

Trophocyte of bud of Ephydatia, 48

Trophozooids of Doliolnm, 640

Trunk blastema, formation of, in the embryo

of Nephdis, 162 ; in the embryo of

Phascolosoma, 375 ; in the larva of /'"f//-

fjurdius, 142

Truuk-coelom, formation of, in A H/JI/H'< >.•'•"••<

lanceolatus, 592 ; in Balanoglossus dam-
gems, 574 ; in Actinotrocha larva of I'lmr-
oitis, 381 ; in New England Tornaria, 575

Tubal cells of archiuephridia in Polyijui'diim,
140

Tube-feet, formation of, in Asterias, 471 ; in
Asterina gibbosa, 476 ; in C/ici/i/inria
planci, 542 ; iu Echinus esculentus, 514,
517 ; in Ophioth /•/.-•. fmyi/ix, 493, 495

Tubularia, 60, 61, 62, 383 ; development of,
54-69

Tubularia indivi-sa, 54

Tubularia mesembryanthcmum., 54

Tunicata, 406, 413, 564, 568, 659, 662,
development of, 608-646

Turbellaria, 102

Turret cells in segmenting eggs of Gastro-
poda, 322

Umbrella, 324

Umbrella cavity, vestigial character of, in

gonophore of Clam, 62 ; in gouophore of

Sertularia, 62 ; formation of, in medusa

of Tubularia, 57
Under-basal plates, formation of, in Amplii-

ura squamata, 499 ; in Antedon rosacea,

548 ; union of, in Antedon rosacea, 558
Uuderlip, formation of, in L'o/liiH /m russeola,

423

Unio, embryonic development of, 351
Uuiouidae, 349, 350, 351, 353, 655
Upper sclerotomes, formation of, in larva of

Amphioxus lanceolatus, 599
Ureter, formation of, in Asfactis, 188 ; in

Dreissensia, 344 ; in Paludina, 314
Urnatella, 398
Urochorda, see Tunicata
Urodela, 656, 657
Urticina crassicornis, 85 ; development of,

76-83
Uterus of A scar is megalocephala, 438

Vagina in Ascaris megalocephala, 438 ; forma-
tion of, in Pedicellina echinata, 401

Valeriauic acid, \ise of, 18

Valve of intestine, formation of, in larva of
PuJi/ijoi-dius, 143

Vas deferens in Ascfiri* megalocephala, 438 ;
formation of, iu Molyula, 628 ; in tii<jitt«
blpunctata, 434

Vegetative pole of the egg denned, 26

Velella, 64

Veliger larva, 416 ; of l^ntnliinn, 329 ; of
Dreissensia, 338 ; of Gastropoda, 369 ; of
Paludina, 310 ; of P«M/,,. 300 ; of Fele-
cypoda, 369 ; of Seapliopoda, 369

Velum, formation of, in larva of (_'rfj>iitnl<t,
321 ; in larva of l>>'iil'tli>nn, 329 : in larva
of />(V/,v.sr//.s/c, 3:J8 ; in larvn of /•'/"/«</,
321 ; in larva of r«trll«, :!00 ; in larva
of Protobranchiata, 319 ; in mtdusa of
Tiiliulid-ia, 58

Vena cava, formation of. in L'/i;/", 362

Ventral blood- \v^ul, formation of, in
x, 518

692

INVEETEBEATA

Ventral cell-family in segmenting egg of

. IMW/-/.S- megalocephala, 4-10
Ventral ciliated epaulettes, formation of, in

larva of Echinus esculentus, 511
Ventral ganglion, formation of, in Say it /it

t>ij»iitct«fn, 432

Ventral nerve-cord, formation of, in Crio-
In, i/nm, 158 ; \\\ Nephelis, 162 ; in
citjiciisis, 174 ; in Polyyon/iiix

147
Ventral organs, formation of, in Peripntnn

rii/ii'iis-is, 174
Ventral plate in the embryo of Agelena, 224 ;

in embryo of Unio, 351
Ventral retractor muscles, formation of, in

larva of /irrissensia, 341
Ventral shield in embryo of Astacus, 186
Ventral sinus, formation of, in J\Vy<//<://X 163
Ventricle of heart, formation of, in Cyr/ax,

350 ; in Loligo, 362
Ventro-lateral chamber of Urticina crussl-

cornis, 80
Vertebra, formation of, in Ampl/iurc xij/itt-

mattt, 499
Vertebrata, 29, 162, 568, 569, 584, 585,

586, 605, 606, 608, 625, 636, 646, 662
Vesicula seminalis of Ascaris megalocephala,

438
Vestibule, formation of, in larva of Antedon

rosacea, 557 ; in larva of Pedicr//i/nt, 400
Vibratile cleft, formation of, in Cyphonautes

larva, 390
Vibratile plume, formation of, in Cyphonautes

larva, 391
Visceral ganglion, formation of, in larva of

simple Ascidian, 622 ; in Dreiwiixin,

342 ; in Loligo, 358 ; in Paluilina, 315
Visceral hump, formation of, in Loligo,

361 ; in I'ntdlu, 300
Visceral muscles, formation of, in CV/W;Y///.s,

158 ; in Jjoni/ciit, 256 ; in Polygordius

appendiculatus, 147
Visual rods, of Cephalopod eye, formation

of, 368 ; of ocelli of Dytiscus, 273, 274
Yitellarium of Gallidina russeola, 424
Vitelligenous cells of Platyhelmiuthes, 102
Vitelline membrane, definition of, 3 ; forma-
tion of, 9, 17; in egg of Ainjil/in.:'".-.

587 ; in unfertilized eggs of Echinoidea,

524
Volvox, 660 ; compared with blastula, 51

Water-tubes of larva of A-stcrias, 466

Water- vascular system of Eehinodermata
see Hydrocoele

Wheel-organ, formation of, in A m/ili 'n>,< u
lanceolatus,6Q<l ; in Callidina /•/'.«<:"/«, 421

Wheels in larva of Syn«j>(it ifigifntii, 535

White bodies, formation of, in Loligo, 361

Wings of Dnri/phura, development of, 271
273

V\ ings, rudiments of, in larva of Galerun-ll,
til mi, 268

Wing-sac of Buprestidae, 277 ; of Ceram
bycidae, 277 ; of Culicidae, 278 ; ii
Doryphora, 271 : in Insecta, various type
of, 277-279 ; of Lepidoptera, 278 ; o
Muscidae, 278, 279 ; of Scarabaeidae
277 ; of Tipulidae, 278

Worm-like larva of Ophium lircrisjiiim, 56:

Xiphosura, 221

yi>l</in, 1 n-va of, 349, 369

Yolk, influence of, on segmentation of egg, an<

on the formation of layers in the embryo

26, 657
Yolk -cells, formation of, in embryo o

Donacia, 247 ; in embryo of /,<y»'.v///«

264 ; in embryo of Pyrosomn, 633 ; ii

Scoloftendra, 282
Yolk-lobe in egg of Dent.alimn, 326. (&•

also Polar lobe.)
Yolk-membrane, formation of, in egg o

Sepia, 355
Yolk-nucleus, definition of, 3 ; of egg o

Cynthia partita, 610
Yolk-sac, development of, in Ifeli.v, 369

in Loligo, 360
Y'linijia, 161 ; development of larva of, 112

115

Zoaea larva, 217 ; description of, 208 ; ii:
terpretation of, 210-212 ; of Anonmni
210, 213 ; of Brachyiira, 210, 213 ; o
Caridea, 209, 213 ; of Euphausidacea
208, 212 ; of Penaeidea, 209, 212

Zoantharia, 53 ; development of, 76-86

Zoanthella larva of Zoanthidae, 85

Zoauthidae, 53 ; larvae of, 85

Zoanthina larva of Cereanthidae, 85

Zocecium, formation of, in Polyzoa Ecto
procta, 396, 397

Zygonema, definition of, 4

Zygote, definition of, 2

Zygote nucleus, definition of, 9

Zygotene thread, definition of, 4

END OF VOL. I

Printed by R. & R. CI.AKK, LIMITKD.

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