Atlas of Comparative Invertebrate Embryology

Volume 1: Porifera, Cnidaria, Ctenophora
Preface 9
Acknowledgement 10
Introduction 11
Characteristics of comparative embryology 11
Biological systematics 12
Eggs and embryos 12
Cleavage 12
Blastula 12
Gastrulation, second germ layer formation 12
Mesoderm, third germ layer formation 13
Organ differentiation 13
Larvae 13
Molecular biology and development 14
Literature 15
Diploblastic Organisms – Animals with two germ layers 16
Phylum Porifera 16
Symplasma* – Class Hexactinellida 16
Cellularia 17
Calcarea 17
Calcaronea 17
Leucosolenia botryoides (ELLIS & SOLANDER) 17
Sycon raphanus (O. SCHMIDT) 20
Grantia compressa (FABRICIUS) 24
Calcinea 26
Ascandra minchini (BOROJEVIC) 26
Clathrina falcata (HAECKEL) 28
Clathrina coriacea (MONTAGU) 28
Demospongiae 30
Homoscleromorpha 30
Oscarella lobularis (O. SCHMIDT) 30
Tetractinomorpha 30
Tethya aurantium (PALLAS) 30
Polymastia robusta (BOWERBANK) 33
Raspailia pumila (BOWERBANK) 34
Ceractinomorpha 35
Myxilla rosea (LIEBERKÜHN) 35
Halisarca dujardini (JOHNSTON) 36
Ephydatia fluviatilis (LINNÉ) 37
Summary of the Ontogenesis in Porifera 40
Cleavage, morula, coeloblastula, amphiblastula 40
Reorganization process of germ layers, parenchymulae, gastrulation, metamorphosis 40
Polarity of the sponge egg and rudiment of germ layers 41
Comparison of ontogenies in Porifera 42
Embryonic development in Porifera and evolutionary interpretation 43
Phylogenetic Transition between Protozoans and Metazoans 44
Comparative embryology 44
Comparative morphology 44
Morphogens 45
Biochemistry of the extracellular matrix 45
Literature 46
Phylum Cnidaria 49
Class Anthozoa 49
Hexacorallia 50
Ceriantharia 50
Cerianthus lloydii (GOSSE) 50
Pachycerianthus multiplicatus (CALGREN) 50
Actinaria 52
Metridium senile var. dianthus (ELLIS) 52
Aiptasia mutabilis (GOSSE) 55
Anthopleura xanthogrammica (BRANDT) 55
Tealia crassicornis (MÜLLER) 56
Madreporaria 56
Favia fragum (ESPER) 56
Platygyra sinensis (EHRENBERG) 57
Zoantharia 58
Protopalythoa spec. 58
Octocorallia 60
Alcyonaria 60
Alcyonium digitatum (LINNÉ) 60
Sympodium coralloides (MILNE EDWARDS) 62
Pennatularia 62
Ptilosarcus guerneyi (GRAY) 62
Helioporida 64
Heliopora coerula (PALLAS) 64
Summary of Ontogenesis in Anthozoa 65
Cleavage and gastrulation 65
Anthozoan larvae 65
Embryonic development in Anthozoa and evolutionary interpretation 66
Comparative embryology 66
Nucleotide sequence data 67
Structure of the mitochondrial genome 67
Literature 67
Class Scyphozoa 69
Coronata 71
Linuche unguiculata (SCHWARTZ) 71
Semaeostomea 71
Chrysaora hysoscella (LINNÈ) 71
Cyanea capillata (LINNÈ) 72
Aurelia aurita (LAMARCK) 73
Rhizostomea 75
Cassiopea andromeda (FORSKAL) 75
Cotylorhiza tuberculata (MACRI) 76
Mastigias papua (LINNÉ) 78
Stauromedusida 78
Haliclystus octoradiatus (LAMARCK) 80
Class Cubozoa 80
Tripedalia cystophora (CONANT) 80
Carybdea rastoni (HAACKE) 82
Summary of Ontogenesis in Scyphozoa and Cubozoa 82
Cleavage and gastrulation 82
Scyphozoan and cubozoan larvae 82
Embryonic development in Scyphozoa and Cubozoa and evolutionary interpretation 82
Comparative embryology 82
Comparative morphology 83
Nucleotide sequence data 83
Literature 83
Class Hydrozoa 84
Hydroidea 84
Thecata – Leptomedusae 84
Aequorea aequorea (PÉRON & LESUEUR) 84
Eucheilota maculata (HARTLAUB) 86
Clytia gregaria (AGASSIZ) 86
Phialidium hemisphaericum (LINNÈ) 87
Obelia longissima (PALLAS) and Obelia geniculata (LINNÉ) 88
Athecata – Anthomedusae 90
Clava multicornis (O. F. MÜLLER) 90
Cordylophora caspia (PALLAS) 93
Podocoryne carnea (SARS) 93
Hydractinia echinata (FLEMING) 96
Eudendrium armatum (TICHOMIROV) 96
Coryne muscoides (LINNÉ) 98
Sarsia eximia (ALLMAN) 100
Tubularia mesembryanthemum (ALLMAN) 100
Tubularia crocea (AGASSIZ) 100
Hydrina 103
Hydra grisea (LINNÉ) 103
Hydra carnea (AGASSIZ) 103
Hydra vulgaris (PALLAS) 104
Lymnohydrina 104
Gonionemus vertens (AGASSIZ) 104
Trachylida 104
Geryonia fungiformis (METSCHNIKOFF) 104
Summary of Ontogenesis in Hydrozoa 106
Cleavage and gastrulation 106
Endoderm 107
Hydrozoan larvae 107
Composition of the extracellular matrix (mesogloea) 107
Embryonic development in Hydrozoa and evolutionary interpretation 107
Literature 108
Class level relationships in the phylum Cnidaria 110
Comparative embryology 110
Comparative morphology 110
Structure of the mitochondrial genome 111
Phylogeny of Cnidaria 111
Literature 111
Phylum Ctenophora 113
Tentaculifera 114
Cydippida 114
Pleurobrachia pileus (O. F. MÜLLER) 114
Callianira bialata (DELLE CHIAJE) 114
Lobata 115
Mnemiopsis leidyi (AGASSIZ) 115
Ocyropsis maculata (RANG) and Ocyropsis crystallina (RANG) 119
Atentaculata 120
Beroida 120
Beroe ovata (CHAMISSO and EYSENHARDT) 120
Summary of the Ontogenesis in Ctenophora 123
Cleavage and gastrulation 123
Embryonic development in Ctenophora and evolutionary interpretation 123
Mesogloea in Ctenophora 123
Comparative embryology 123
Comparative morphology 124
Nucleotide sequence data 124
Literature 124
Phylum Placozoa 126
Literature 126
Ancestral mode of ontogeny in diploblastic animals 127
Cleavage pattern 127
Gastrulation 127
Second germ layer hypothesis 127
The bilaterogastraea-theory 130
Blastopore formation 130
Phylum-level relationships, molecular biology and traditional homology 131
Protostomia versus Deuterostomia 131
Comparative embryology 131
Molecular biology 131
Developmental genetics and “homology” 132
Literature 132
Glossary 135

Volume 2: Hemichordata (Enteropneusta, Pterobranchia)
Triploblastic Organisms – Animals with three germ layers 7
Archicoelomata 7
Phylum Hemichordata 7
Class Enteropneusta 8
Ptychoderidae 8
Balanoglossus clavigerus (DELLE CHIAJE) 8
Ptychodera bahamensis (SPENGEL) 12
Ptychodera flava laysanica (SPENGEL) 19
Glossobalanus minutus (KOWALEVSKY) 22
Spengeliidae 22
Glandiceps stiasnyi (RAO) 22
Harrimaniidae 25
Saccoglossus kowalevskii (AGASSIZ) 25
Saccoglossus otagoensis (BENHAM) 32
Saccoglossus horsti (BRAMBELL & GOODHART) 33
Summary of Ontogenesis in Enteropneusta 37
Cleavage, gastrulation and mesoderm formation 37
Larvae 38
Embryonic development in Enteropneusta and evolutionary interpretation 40
Formation of the mesoderm germ layer 40
Tornaria larva 40
Class-level relationship of Enteropneusta 40
Literature 41
Class Pterobranchia 43
Rhabdopleurida 43
Rhabdopleura normani (ALLMAN) 43
Rhapdopleura compacta (HINCKS) 47
Cephalodiscus gilchristi (RIDEWOOD) 50
Cephalodiscus indicus (SCHEPOTIEFF) and Cephalodiscus nigrescens (LANKESTER) 53
Summary of Ontogenesis in Pterobranchia 54
Cleavage, gastrulation and mesoderm formation 54
“Larvae” 54
Embryonic development in Pterobranchia, larval and adult morphology, and evolutionary interpretation 55
Embryology 55
Larval and adult morphology and class-level relationship of Pterobranchia 55
Prosoma 55
Mesosoma 56
Metasoma 56
Literature 57
Phylum Level Relationships of Hemichordata 59
Larval types 59
Larval and adult morphology 59
Prosoma 59
Heart-glomerulus complex in hemichordates 59
Heart-glomerulus complex in echinoderms 61
Stomochord 62
Preoral ciliary organ 62
Mesosoma 63
Nervous system 63
Lophophore 63
Lophophore and molecular systematics 64
Metasoma 64
Gill slits 64
Summary 66
Literature 67
Glossary 70

Volume 3: Lophophorata (Phoronida, Brachiopoda, Bryozoa)
Phylum Lophophorata 8
Class Phoronida 8
Phoronis buskii (McINTOSH) 9
Phoronis muelleri (de SELYS-LONGCHAMPS) 15
Phoronis psammophila (CORI) 19
Phoronis vancouverensis (PIXELL) 23
Phoronis ovalis (S. WRIGHT) 25
Phoronopsis harmeri (PIXELL) 27
Summary of Embryonic Development in Phoronida 30
Fertilization, cleavage and gastrulation 30
Mesoderm formation in larva 30
Larva 31
Metamorphosis 32
Embryonic development in Phoronida 32
Class- and phylum-level relationships of Phoronida 33
Prosoma 33
Mesosoma 34
Metasoma 34
Nervous system of the actinotrocha 35
Ciliary bands 35
Literature 36
Class Brachiopoda 38
Ecardines 39
Lingula unguis (LINNÉ) 39
Glottidia pyramidata (STIMPSON) 41
Discinisca strigata (BRODERIP) 44
Discinisca atlantica (KING) 46
Crania anomala (O. F. MÜLLER) 48
Testicardines 52
Notosaria nigrcans (SOWERBY) 52
Terebratulina septentrionalis (COUTHOUY) 55
Terebratulina retusa (LINNÉ) 60
Argyrotheca cordata (RISSO) 63
Waltonia inconspicua (SOWERBY) 65
Pumilus antiquatus (ATKINS) 68
Terebratalia transversa (SOWERBY) 70
Summary of Embryonic Development in Brachiopoda 73
Embryonic development 73
Larval development in Testicardines 73
Juvenile development in Ecardines: Lingula, Glottidia, and Discinisca 74
Larval development in Ecardines: Crania 75
Adult morphology, embryonic and larval development in Brachiopoda and evolutionary interpretation 75
Morphology 75
Embryology 76
Larvae and juveniles 76
Class and phylum level relationship of Brachiopoda 77
Mode of mesoderm formation 77
Protocoel and prosoma 77
Apical ganglion 77
Mesocoel and lophophore 78
Metacoel and metasoma 78
Literature 79
Class Bryozoa 82
Gymnolaemata 83
Ctenostomata – species with planktotrophic shelled cyphonautes larvae 83
Alcyonidium albidum (ALDER) 83
Hypophorella expansa (EHLERS) 85
Farrella repens (FARRE) 86
Ctenostomata – species with lecithotrophic shelled coronate larvae 87
Flustrellidra hispida (FABRICIUS) 87
Pherusella tubulosa (ELLIS & SOLANDER) 94
Ctenostomata – species with lecithotrophic coronate larvae without shell 95
Alcyonidium gelatinosum (LINNÉ) 95
Triticella flava (DALYELL) 100
Bowerbankia gracilis (LEIDY) 101
Bulbella abscondita (BRAEM) 106
Victorella muelleri (KRAEPELIN) 106
Paludicella articulata (EHRENBERG) 109
Cheilostomata 110
Anasca – species with planktotrophic shelled cyphonautes larvae 110
Electra pilosa (LINNÉ) 110
Membranipora membranacea (LINNÉ) 115
Electra crustulenta (PALLAS) 118
Electra monostachys (BUSK) 120
Conopeum seurati (CANU) 120
Conopeum reticulum (LINNÉ) 120
Anasca – species with lecithotrophic coronate larvae 120
Bugula flabellata (THOMPSON) 120
Bugula neritina (LINNÉ) 123
Tricellaria occidentalis (TRASK) 128
Cheilostomata 129
Ascophora – species with lecithotrophic coronate larvae 129
Watersipora cucullata (BUSK) 129
Watersipora arcuata (BANTA) 130
Stenolaemata 132
Stenostomata – species with polyembryony and lecithotrophic coronate larvae 132
Crisia ramosa (HARMER) 132
Crisia eburnea (LINNÉ) 135
Lichenopora verrucaria (FABRICIUS) 137
Phylactolaemata 141
Plumatella fungosa (PALLAS) 141
Fredericella sultana (BLUMENBACH) 146
Summary of Embryonic Development in Bryozoa 151
Gametes and fertilization 151
Brooding mechanisms in Gymnolaemata 151
Brooding mechanisms in Stenolaemata 152
Brooding mechanisms in Phylactolaemata 152
Embryogenesis in Gymnolaemata 153
Cleavage and gastrulation 153
Larvae of Gymnolaemata 153
Cyphonautes larvae 153
Coronate larvae 154
Metamorphosis of gymnolaemate larvae 155
Embryogenesis in Stenolaemata 155
Embryogenesis in Phylactolaemata 156
Embryonic development in Bryozoa and evolutionary interpretation 156
Hypothetical gymnolaemate larva 157
Coelom cavities in bryozoan larvae 157
Class level relationships of Bryozoa 158
Embryonic and larval features 158
Biradial symmetry in cleavage 158
Endoderm and digestive tract 158
Mesoderm and coelom 158
Metasomal or adhesive sac 159
Pyriform organ 159
Larval corona 159
Ciliated ridge of cyphonautes 160
Adult features 160
Lophophore 160
Coelom cavities 160
Phylum level relationships of Bryozoa 161
Literature 162
Glossary 167
zum Anfang

Volume 4: Echinodermata I (Crinoidea, Asteroidea, Ophiuroidea)
Phylum Echinodermata 7
Class Crinoidea 7
O. Isocrinida 8
Metacrinus rotundus (CARPENTER) 8
O. Comatulida 9
Oxycomanthus japonicus (MÜLLER) 9
Antedon mediterranea (LAMARCK) 13
Tropiometra carinata (Lamarck) 18
Compsometra serrata (A. H. CLARK) 22
Isometra vivipara (MORTENSEN) 24
Notocrinus virilis (MORTENSEN) 26
Florometra serratissima (A. H. CLARK) 28
Summary of Embryonic Development in Crinoidea 31
Brooding, cleavage type, coelomogenesis, and organ differentiation 31
Larval types and metamorphosis 31
Class level relationship 32
Literature 32
Class Asteroidea 33
O. Paxillosida 34
Astropecten aranciacus (LINNÉ) 34
Astropecten irregularis (LINCK) 42
Astropecten scoparius (VALENCIENNES) 43
Astropecten latespinosus (MEISSNER) 46
Astropecten gisselbrechti (DÖDERLEIN) 47
Luidia quinaria (VON MARTENS) 49
O. Valvatida 52
Asterina pectinifera (MÜLLER & TROSCHEL) 52
Asterina gibbosa (PENNANT) 54
Asterina batheri (GOTO) 65
Asterina minor (HAYASHI) 69
Asterina pseudoexigua pacifica (HAYASHI) 72
Porania pulvillus (O. F. MÜLLER) 72
Odontaster validus (KOEHLER) 76
Acanthaster planci (LINNÉ) 77
Archaster typicus (MÜLLER & TROSCHEL) 78
Patiriella regularis (VERRILL) 80
Patiriella pseudoexigua (DARTNALL) 83
Patiriella exigua (LAMARCK) 84
Patiriella vivipara (DARTNALL) 89
O. Velatida 89
Solaster endeca (FORBES) 89
Crossaster papposus (MÜLLER & TROSCHEL) 94
Pteraster tesselatus (YVES) 98
O. Spinulosida 103
Henricia sanguinolenta (MÜLLER) 103
Echinaster echinophorus (LAMARCK) 107
O. Forcipulatida 109
Asterias vulgaris (PACKARD) 109
Asterias rubens (LINNÉ) 111
Leptasterias hexactis (STIMPSON) 118
Stichaster australis (VERRILL) 123
Summary of Embryonic Development in Asteroidea 126
Brooding, cleavage type, coelomogenesis, and organ formation 126
Larval types of asteroids 126
Metamorphosis 127
Asteroid larval types and evolutionary interpretation 127
Class level relationship of asteroids 128
Literature 128
Class Ophiuroidea 130
O. Phrynophiurida 131
Ophiomyxa brevirima (H. L. CLARK) 131
Gorgonocephalus eucnemis (MÜLLER & TROSCHEL) 131
O. Ophiurida 132
Ophiolepis elegans (LÜTKEN) 132
Ophiocoma nigra (ABILDGAARD) 133
Ophiocoma pumila (LÜTKEN) 137
Ophioderma brevispina (SAY) 138
Ophioderma longicauda (RETZIUS) 143
Ophionereis annulata (LE CONTE) 145
Amphiura chiajei (FORBES) 145
Amphipholis kochii (LÜTKEN) 146
Amphipholis japonica (MATSUMOTO) 148
Amphipholis squamata (DELLE CHIAJE) 150
Amphioplus abditus (VERRILL) 153
Ophiothrix fragilis (ABILDGAARD) 154
Ophiothrix suensoni (LÜTKEN) 158
Ophiothrix oerstedi (LÜTKEN) 158
Ophioplutei 160
Summary of Embryonic Development in Ophiuroidea 165
Brooding, cleavage type, coelomogenesis, and organ formation 165
Larval types in ophiuroids 165
Metamorphosis 166
Ophiuroid larval types and evolutionary interpretation 166
Literature 167
Glossary 168

Volume 5: Echinodermata II (Echinoidea, Holothuroidea)
Phylum Echinodermata 7
Class Echinoidea 7
Subclass Cidaroidea 8
O. Cidaroida 8
Eucidaris metularia (LAMARCK) 8
Eucidaris tribuloides (LAMARCK) 9
Eucidaris thouarsi (VALENCIENNES) 10
Prionocidaris baculosa (LAMARCK) 13
Phyllacanthus imperialis (BRANDT) 15
Phyllacanthus parvispinus (LAMARCK) 17
Subclass Euechinoidea 19
O. Echinothurioida 19
Asthenosoma ijimai (YOSHIWARA) 19
O. Diadematoida 21
Diadema setosum (LESKE) 21
O. Temnopleurida 24
Temnopleurus toreumaticus (KLEIN) 24
Toxopneustes pileolus (LAMARCK) 24
Tripneustes gratilla (LINNÉ) 25
Mespilia globulus (AGASSIZ) 26
Holopneustes purpurescens (AGASSIZ) 28
O. Echinoida 31
Echinus esculentus (LINNÉ) 31
Paracentrotus lividus (LAMARCK) 37
Pseudocentrotus depressus (AGASSIZ) 41
Strongylocentrotus pulcherrimus (AGASSIZ) 41
Strongylocentrotus droebachiensis (O. F. MÜLLER) 44
Psammechinus miliaris (GMELIN) 45
Echinometra Mathaei (BLAINVILLE) 49
Echinostrephus moralis (AGASSIZ) 49
Heliocidaris erythrogramma (VALENCIENNES) 50
O. Clypeasteroida 55
Clypeaster humilis (LESKE) 55
Echinocyamus pusillus (O. F. MÜLLER) 56
Laganum depressum (AGASSIZ) 60
Peronella japonica (MORTENSEN) 61
O. Spatangoida 63
Lovenia elongata (GRAY) 63
Brissopsis lyrifera (FORBES) 64
Summary of Embryonic Development in Echinoidea 65
Egg size, cleavage, coelomogenesis, organ formation, and metamorphosis 65
Phylogenetic relationships of the Echinoidea 66
Literature 66
Class Holothuroidea 68
O. Dendrochirotida 69
Cucumaria doliolum (?) 69
Cucumaria planci (BRANDT) 71
Cucumaria glacialis (LJUNGMAN) 72
Cucumaria normani (?) and Cucumaria saxicola (BRADY & ROBERTS) 73
Cucumaria elongata (DÜBEN & KOREN) 74
Phyllophorus urna (GRUBE) 76
Thyone briareus (LESEUR) 76
O. Aspidochirotida 78
Opheodesoma grisea (SEMPER) 78
Holothuria tubulosa (GMELIN) 78
Holothuria impatiens (FORSKAL) 80
Holothuria floridana (POURTALÉS) 81
Holothuria papillifera (HEDING) 83
Stichopus tremulus (GUNNERUS) 83
Stichopus californicus (?) 84
Actinopyga serratidens (PEARSON) 87
O. Apodida 88
Labidoplax buskii (M’INTOSH) 88
Synapta vivipara (ÖRSTED) 91
Synaptula vittata (FORSKAL) 93
Chiridota rotifera (POURTALÉS) 95
Trochodota dunedinensis (PARKER) 96
Rhabdomolgus ruber (KEFERSTEIN) 96
O. Molpadiida 96
Molpadia intermedia (LUDWIG) 96
Summary of Embryonic Development in Holothuroidea 99
Cleavage, gastrulation, and coelomogenesis 99
Indirect development, larvae and metamorphosis 99
Direct development and the doliolaria larva 100
Brooding 100
Phylogenetic relationships of the Holothuroidea 102
Literature 103
Glossary 105
Comparative Embryology and the Archicoelomata Theory 106
Larvae of Archicoelomata 106
Phylum-level relationships and animal superphyla 107
Literature 108

Dr. Martin E. L. SCRIBA
Professor of Zoology
Born 1931
Teaching zoology, embryology and evolution in years
1968-1971
Philipps-University of Marburg, Germany
1971-1996
University of Aachen, Germany (RWTH)

How should I use my time after retirement?
To realize my dream of writing this atlas of comparative Embryology
Why an atlas?
People prefer to visualize ideas so on an atlas is an ideal method of presenting different processes of embryological development.
Why compare embryological development in different taxonomic groups such as families, orders and classes?
Because closely related organism pass through simple and highly determined embryonic development. At the end of some chapters the relevant results of research in development biology using gene sequence data, gene expression and protein chemistry are discussed.
What is the scope of the atlas?
The atlas presents an extensive illustrated compilation of embryonic development in animal phyla, it refers to publications about embryology from the 1860‘s until the present day. It is concerned with descriptive embryology, looking at the composition of embryos and larvae and their morphological changes during development.
What is the aim of the atlas?
Comparative embryology allows the construction of phylogenetic trees. The atlas supports the Gastraea-theory of HAECKEL (1874) and the Archicoelomata-theory of MASTERMAN (1898).