Comparative anatomy of the foramen ovale in the hearts of cetaceans.

The structure of the cardiac foramen ovale from 17 species representing six cetacean families, the Monodontidae, Phocoenidae, Delphinidae, Ziphiidae, Balaenidae and the Balaenopteridae, was studied using the scanning electron microscope. Eight white whale fetuses (Delphinapterus leucas) and a narwhal fetus (Monodon monoceros) represented the Monodontidae; one fetal and nine neonatal harbour porpoises (Phocoena phocoena) and a finless porpoise fetus (Neophocoena phocoenoides) represented the Phocoenidae; two white-beaked dolphin fetuses (Lagenorhynchus albirostris), four fetal and one neonatal Atlantic white-sided dolphins (Lagenorhynchus acutus), a Risso's dolphin fetus (Grampus griseus), two common bottle-nosed dolphin neonates (Tursiops truncatus), a female short-beaked common dolphin fetus (Delphinus delphis), four killer whale fetuses (Orcinus orca) and two long-finned pilot whale fetuses (Globicephala melas) represented the Delphinidae; two northern bottlenose whale fetuses (Hyperoodon ampullatus) represented the Ziphiidae; one bowhead whale fetus (Balaena mysticetus) represented the Balaenidae and five Common minke whale fetuses (Balaenoptera acutorostrata), one blue whale fetus (Balaenoptera musculus), nine fin whale fetuses (Balaenoptera physalus) and four humpback whale fetuses (Megaptera novaeangliae) represented the Balaenopteridae. The hearts of an additional two incompletely identified toothed and four baleen whale fetuses were also studied. In each species the fold of tissue derived from the cardiac septum primum and subtended by the foramen ovale had the appearance of a short tunnel or sleeve which was fenestrated at its distal end. In the toothed whales the tissue fold was tunnel-shaped with the interatrial septum as the floor whereas in baleen whales it was more sleeve-like. In toothed whales thin threads extended from the fold to insert into the interatrial septum whereas a network of threads covered the distal end of the sleeve in the baleen whales. Similar structures were present in the corresponding cardiac tissues of neonatal Hippopotamidae.

[Comparative analysis of vestibular system development in various groups of mammals living under different environmental conditions]. / Cravnitel'nyi analiz razvitia vestibularnogo apparata mlekopitaushchix s razlichnoi c'kologiei.

We have conducted for the first time a comparative study of the prenatal development of the vestibular system in representatives of pinnipeds (Phocidae, Otariidae, Odobenidae) and cetaceans (Odontoceti, Mysticeti) in comparison with terrestrial mammals. This allowed us to perform a detailed study of the structural organization of the inner ear in species with different ecological specialization, to find out adaptive aspects and stages of the formation of cochlear and vestibular structures in each of the studied species, and to correlate it with the properties of the environment. Studies on early embryogenesis of the labyrinth in cetaceans and pinnipeds, which represent a special direction in the evolution of placentates, give a significant contribution to the solution of problem about the evolutionary origin of the labyrinth in mammals studied. Sensory systems clearly demonstrate the scope of evolutionary and adaptive transformations, which appear in mammals during the transition from the terrestrial to the aquatic mode of life. At the same time, these results may provide help in understanding the general trends of the development of structure and function of the inner ear in mammals as a whole.

Development of the cetacean nasal skull.

The adaptation of cetaceans to aquatic life habits is reflected, in their nasal region, in three marked changes from the original relations found in land mammals. These changes include (1) the loss of the sense of smell, (2) translocation of the nostrils from the tip of the rostrum to the vertex of the head, and (3) elongation of the anterior head to form a rostrum protruding far towards anterior. The morphogenetic processes taking place during embryogenesis of the nasal skull play a decisive part in the development of all these changes. The lateral parts of the embryonic nasal capsule, encompassing the nasal passages, change their position from horizontal to vertical. At the same time, the structures of the original nasal floor (the solum nasi) are shifted in front of the nasal passages towards the rostrum. The structures of the original nasal roof (the tectum nasi) and of the nasal side wall (the paries nasi) are translocated behind the nasal passages towards the neurocranium. The medial nasal septum (the septum nasi) mostly loses its connection to the nasal passages and is produced into a point protruding far towards anterior. The transformed embryonic nasal skull of the Cetacea can be divided into three sections: 1. The median structures. These include the cartilaginous structures, viz., the rostrum nasi, the septum interorbitale and the spina mesethmoidalis, which are accompanied by the dermal bones, the vomer and the praemaxillare. In adult cetaceans the rostrum nasi is mostly preserved as a robust cartilage of the skull, which may possibly serve as a sound transmitting structure of the sonar system, or it may be responsible for the sensing of water streams and vibrations. 2. The posterior side wall structures. These include the following cartilaginous structures that are mostly heavily reduced or mutually fused: the cupula nasi anterior, the tectum nasi, the lamina cribrosa, the paries nasi, the commissura orbitonasalis, the cupula nasi posterior, the processus paraseptalis posterior, the crista semicircularis, the frontoturbinale, the ethmoturbinale I and the maxilloturbinale. The cartilaginous structures are largely accompanied by the dermal bone, the maxillare. Of these embryonic elements, very little is preserved in adult cetaceans. The cartilages of the cupula nasi anterior form the variable skeleton around the nostrils. In Physeter the tectum nasi forms a very long cartilaginous bar that passes through the whole giant anterior head of the sperm whale as a structure accompanying the left nasal passage. 3. The anterior side wall structures. These include the cartilaginous structures, viz., the cartilago ductus nasopalatini, the cartilago paraseptalis, the processus lateralis ventralis and the lamina transversalis anterior, accompanied by the dermal bones, the praemaxillare and the vomer. These structures participate in the formation of the robust rostrum of the cetacean skull, and they are partly preserved even in adults in the form of the isolated ossa pararostralia (the Meckelian ossicles). The comparison of morphogeny of the nasal skull has also made it possible to draw certain conclusions on the phylogeny and systematics of Cetacea. Already the earliest embryonic stages permit us to discern weighty transformations of the original nasal skull of land mammals. These transformations are common to all embryos examined. This fact indicates a common origin of all Cetacea, which thus form a single monophyletic order. However, later embryonic stages show some different modifications of the nasal capsule according to which at least three major groups can be distinguished within the order Cetacea, probably ranking as superfamilies: Balaenopteroidea, Physeteroidea and Delphinoidea. Our observations, being in full accordance with other morphological, and embryological, as well as molecular biological results, suggest that the division of the order Cetacea into two suborders, Mysticeti and Odontoceti, is no longer tenable.

Studies on the fetal development of the gubernaculum in cetacea.

BACKGROUND: Adult cetacean males, like non-mammalian vertebrates and other testicond mammals, have intra-abdominal testes. There is no evidence of a processus vaginalis in them. Testicondia in cetaceans is considered secondary as they are judged, evolutionarily, the descendants of terrestrial mammals (ungulates) with testis descent. A possible argument in support of the latter contention would be that cetacean fetuses develop gubernacula which are the primordia of the processus vaginalis and other structures associated with testis descent in other placental mammals. The present study intended to analyse cetacean fetuses in this respect. METHODS: Serial sections of 25 fetuses (total body length between 39.5 and 160 mm) of 4 cetacean species (Delphinus delphis, Phocoena phocoena, Eschrichtius robustus, Physeter catodon) were examined with special attention to the presence or absence of structures homologous to the gubernaculum of other placental mammals (rats and humans). RESULTS: Gubernacular primordia were observed in fetuses from about the time of onset of sexual differentiation. Their shape and anatomical relationship with the surrounding structures were similar as those in mammals with testis descent. The gubernaculum in males developed into a large mass of dense connective tissue in the ventral-caudal abdominal region at the site of the insertion of the mesonephric inguinal ligament and associated to the tip of the internal abdominal oblique muscle. No (or only very little) development of a processus vaginalis was noticed. CONCLUSIONS: The results demonstrate initial emergence of mammalian-like gubernacular primordia in cetacean fetuses without their further development to elaborate structures required for testis descent. The findings support the view that cetaceans are secondarily testicond. It is suggested that (1) absence of the pelvic girdle together with (2) the development of structures in and beyond the caudal abdominal region, particularly the caudal hypaxial musculature, precludes the outgrowth, into caudal direction, of hollow organs (such as the processus vaginalis) from the abdominal cavity.

[A comparative morphological analysis of the development of the ear in mammals]. / Sravnitel'no-morfologicheskii analiz razvitiia organa slukha u mlekopitaiushchikh.

This paper is the first comparative study into prenatal ontogenesis of the peripheral auditory system in mammals. A wide range of ecologically different species was studied, including terrestrial, semi-aquatic and aquatic forms with auditory systems functioning at low, medium, and high frequencies. Structural peculiarities of the development of auditory organ were determined for each studied species in relation to its operation frequency and acoustic properties of the outer medium. The origin and individual stages of morphological adaptations found in semi-aquatic, aquatic, and echolocating species are described. The data obtained allowed to reveal general principles of development of the peripheral auditory system in mammals with different ecological specialization.

Early development of the olfactory and terminalis systems in baleen whales.

The development of the olfactory and terminalis systems was studied in tissue from eight embryonic and early fetal specimens belonging to three species of baleen whales. In contrast to toothed whales, baleen whales, particularly in these ontogenetic stages, are much less specialized in nasal organ morphology. The nasal cavity and peripheral olfactory system are well developed and do not show signs of reduction. However, as in toothed whales, there is no trace of a vomeronasal organ or nerve. The terminalis neuroblasts can already be distinguished from the olfactory material in the embryonic period, and they form compact masses medial and caudal to the developing olfactory bulb. As in most prenatal toothed whales, there are two large intrameningeal terminalis ganglia. These are connected with the telencephalic wall by central rootlets and with the septal mucosa by fiber bundles running through the level of the future cribriform plate. Clusters of terminalis neuroblasts also lie near the septal mucosa and along the peripheral terminalis fiber bundles. The functional implications of the olfactory and terminalis systems in whales are discussed.

Developmental changes of the fore- and hind-limbs in the fetuses of the southern minke whale, Balaenoptera acutorostrata.

15 fetuses of southern minke whale, Balaenoptera acutorostrata (from 8.2 mm C.R.L. to 38.9 mm C.R.L.), obtained from the Kyodo whale company in Japan (in whaling seasons from 1982 to 1986), were used for the present study. The fore-limb first appears in the 11.4 mm fetus, and the hind-limb in the 15.3 mm fetus. The fore-limb develops progressively during gestation, while the hind-limb disappears by the 38.9 mm fetus. The critical period of limb development in southern minke whale was shown to be at a stage between that in the small sized species; Common Porpoise, Phocoena communis and Striped Dolphin, Prodelphinus caeruleoalbus, and in large one; Humpback Whale, Megaptera nodusa.

Development of the external genitalia in fetuses of the southern minke whale, Balaenoptera acutorostrata.

The developmental changes of the anogenital distance and external genitalia were studied in 81 fetuses of the southern minke whale. It was difficult to sex the fetuses with less than 55.8 mm crown-rump length (CRL) even by histological means, but it was easy in the fetuses with more than 77.0 mm CRL and less than 110.0 mm CRL. The histologically determined male fetuses had a ratio of anogenital distance to CRL or body length of more than 5%, while females had a value of less than 4%. At later stages with a CRL of more than 113.0 mm, male fetuses had an umbilicus-directed genital tubercle, while in females a tail-directed tubercle was observed. The present study suggests that the stage with sexual dimorphism might be earlier in the southern minke whale than that previously reported.

Morphogenesis of the digestive tract in the fetuses of the southern minke whale, Balaenoptera acutorostrata.

Gross and histological observations on the digestive tract in 15 fetuses of the southern minke whale (Balaenoptera acutorostrata) with C.R.L. from 37.2 to 1,940mm revealed that the fetal stomach formation in this species resembled that of the ruminant, i.e., the compartment 1 arose from the stomach bud, but not from the esophagus to form the forestomach. The differentiated gastric glands, the parietal cells, were detected in fetuses with more than 213.0mm C.R.L. The circular folds resembling intestinal haustra like circular folds without tenia were detected on the cecum in fetuses with more than 650mm C.R.L. and less than 1,070mm C.R.L. The similar structure was seen in large intestine in fetuses with more than 650mm C.R.L.

Development of the nervus terminalis in mammals including toothed whales and humans.

The early ontogenesis and topography of the mammalian terminalis system was investigated in 43 microslide series of toothed whale and human embryos and fetuses. In early embryonal stages the development of the nasal pit, the olfacto-terminalis placode, and the olfactory bulb anlage is rather similar in toothed whales and humans. However, toothed whales do not show any trace of the vomeronasalis complex. In early fetal stages the olfactory bulb anlage in toothed whales is reduced and leaves the isolated future terminalis ganglion (ganglia) which contains the greatest number of cells within Mammalia. The ganglion is connected with the nasal mucosa via peripheral fiber bundles and with the telencephalon via central terminalis rootlets. The functional implications of the terminalis system in mammals and its evolution in toothed whales are discussed. Obviously, the autonomic component has been enlarged in the course of perfect adaptation to an aquatic environment.

Ontogenetic development of the nervus terminalis in toothed whales. Evidence for its non-olfactory nature.

For the first time in cetaceans, the development of the terminalis system and its continuity between the olfactory placode and the telencephalon has been demonstrated by light microscopy. In the early development of toothed whales (Odontoceti) this system is partially incorporated within the fila olfactoria which grow out from the olfactory placode. As the peripheral olfactory system is reduced in later stages, a strongly developed ganglionlike structure (terminalis ganglion) remains within the primitive meninx. Peripherally it is connected via the cribriform plate with ganglionic cell clusters near the septal mucosa. Centrally it is attached to the telencephalon (olfactory tubercle, septal region) by several nerve fibre bundles. In contrast to all other mammalian groups, toothed whales and dolphins are anosmatic while being totally adapted to aquatic life. Therefore the remaining ganglion and plexus must have non-olfactory properties. They may be responsible for the autonomic innervation of intracranial arteries and of the large mucous epithelia in the accessory nasal air sacs. The morphology, evolution and functional implications of the terminalis system in odontocetes and other mammals are discussed.

[Morphogenesis of the highly specialized nasal skull in the sperm whale (Physeter macrocephalus). I]. / Die Entwicklung des hochspezialisierten Nasenschädels beim Pottwal (Physeter macrocephalus). Teil I.

Investigated the morphogenesis of the nasal structures of the chondrocranium and determatocranium in 15 embryos and foetuses of the sperm whale (Physeter macrocephalus). In the very early stages of the morphogenesis, the nasal capsule of Physeter shows a conspicuous similarity with that of all other odontocetes. In the following stages there are some important differences. Most peculiar is the occurrence of the cartilaginous tectum nasi with the cupulae nasi anteriores, elements which are reduced in all other odontocetes. This cartilaginous complex as a slender band projects obliquely forward from the upper edge of the anterior septal margin. It is free, i.e. not accompanied by membraneous bones. The complex represents the most important factor in the morphogenesis and growth of the characteristic big forehead in Physeter, which contains the spermaceti organ unique within the odontocetes. Other important differences concern the changes in the orientation of the nasal passages and the adjacent skeletal structures. Nevertheless, these differences have to be taken as specializations related to the development of the far-advanced spermaceti organ. As a whole, the embryonic nasal structures in Physeter belong to the same general type of nasal capsule which is common to all odontocetes. The results presented here suggest a close phylogenetic relationship between Physeter and the other Odontoceti.

Morphogenesis and morphology of the brain stem nuclei of Cetacea. II. The nuclei of the accessory, vagal and glossopharyngeal nerves in baleen whales.

The development and final structure of the IXth, Xth and XIth cranial nerve nuclei are studied in ironhematoxylin -, thionin - and protargol -stained serial sections of about 50 baleen whale fetuses (blue whale, Balaenoptera musculus, and fin whale, Balaenoptera physalus ) and one adult fin whale. The nucleus ambiguus is composed of three subdivisions, oral, intermediate and caudal, the last mentioned being contiguous caudally with the dorsal motor Xth nucleus. The oral division develops as three parallel cell columns which merge into a well circumscribed solitary structure with a rostrally expanded "head". It is composed of medium-sized multipolar neurons in a myelin-poor neuropil. In the fin whale a minor group of larger cells is found medial to the "head". In both species a peculiar small-celled nucleus rich in capillaries is found ventral to the "head". The intermediate division initially contains a lateral cell column and a medial region of scattered cells. The lateral column persists throughout life, while the medial field develops into three columns only one of which remains distinct in mature individuals. The cells are larger than in the oral division with the largest cells in the medial column. The two columns are surrounded by a field of scattered neurons which continues without a sharp border into the caudal division which is composed of scattered cells throughout. In its rostral half the cells are of the same multipolar type as in the intermediate division while caudally they appear flattened in the horizontal plane. The dorsal motor Xth nucleus develops as three longitudinal columns. In the fetal brain these are cytologically distinct due to different proportions of small, medium-sized and larger multipolar neurons. The spindle-shaped ventromedial column extends the entire length of the nucleus. It is composed mostly of small to medium-sized cells which caudal to the obex are elongated parallel with the neuroaxis . The dorsolateral and ventrolateral columns are restricted to the middle 1/3 of the nucleus, except in the blue whale where the former extends somewhat more rostrally. They are both characterized by the presence of large multipolar cells, the largest of which are found in the ventrolateral column. In adult specimens the cells are more equally sized and the columnar organization less distinct. The nucleus of the tractus solitarius is of about the same length as the two above mentioned nuclei. Except at the very early stages, the nucleus is ill-defined.(ABSTRACT TRUNCATED AT 400 WORDS)

Morphogenesis and morphology of the brain stem nuclei of Cetacea. I. The hypoglossal nucleus.

1. The hypoglossal nucleus of whalebone whales is composed of four major subdivisions, forming four parallel columns, here called the dorsomedial, the dorsolateral, the ventromedial and the ventrolateral XII columns. 2. The ventromedial XII column extends throughout the hypoglossal nucleus, forming in whalebone whales the rostral as well as the caudal end of the nucleus. 3. The ventrolateral XII column is lamelliformed and splits into a dorsomedial and a ventrolateral part, the former intimately related topographically to the dorsomedial column. 4. The dorsomedial XII column is torpedo-shaped, tapering in rostral direction and terminating a little short of the rostral end of the ventromedial XII column, while the blunt end terminates immediately caudal to the obex. 5. The dorsolateral XII column is the shortest subdivision, approximately one fourth of the length of the entire hypoglossal nucleus. The blunt rostral end of the torpedo-shaped column blends with the dorsomedial XII column, its tapering caudal end terminating rostral to the obex. 6. The cells of the hypoglossal nucleus vary in size from small to medium-sized and large, the small ones dominating in the dorsomedial, the large ones in the dorsolateral and ventromedial XII columns. The ventrolateral column is characterized by spindle-shaped cells. 7. In the toothed whale Phocaena communis the differentiation of the hypoglossal nucleus is less clearcut than in whalebone whales, but a similar structural priniciple is recognizable.