Helmut A. Oelschläger

Development and rudimentation of the peripheral olfactory system in the harbor porpoise Phocoena phocoena (Mammalia: Cetacea)

Serial sections of 13 embryos and fetuses of the harbor porpoise from 10 mm crown‐rump length up to 167 mm total length were studied. Unlike the adult animals, ontogenetic stages of 18–27 mm crown‐rump length still show a typical mammalian olfactory bulb. The olfactory bulb primordium is penetrated by olfactory nerve fibers, the latter passing through the cribriform plate. However, the olfactory bulb anlage is gradually reduced in later stages, its placodal component being largely uncoupled from the telencephalon. As a ganglionlike structure, the remains of the placodal component stay in contact with the nasal septum and mucosa via thin bundles of nerve fibers. The ganglion and plexus can be traced within the meninges until the adult stage of the porpoise. There is strong evidence that they represent the material of the terminalis system, which cannot be distinguished from the olfactory system in earlier stages. A vomeronasal organ could not be detected in the embryonal and fetal material investigated.

Time, pattern, and heterochrony: a study of hyperphalangy in the dolphin embryo flipper

SUMMARY The forelimb of whales and dolphins is a flipper that shows hyperphalangy (numerous finger bones). Hyperphalangy is also present in marine reptiles, including ichthyosaurs and plesiosaurs. The developmental basis of hyper‐phalangy is unclear. Kükenthal suggested that phalanx anlagen split into three pieces during cetacean development, thereby multiplying the ancestral number. Alternatively, Holder suggested that apical ectodermal ridge (AER)‐directed limb outgrowth might be prolonged by a timing shift (heterochrony), leading to terminal addition of extra phalanges. We prepared a series of whole mounted and serially sectioned embryonic flipper buds of the spotted dolphin Stenella attenuata. This cetacean shows marked hyperphalangy on digits II and III. We confirm previous reports that the proximodistal laying down of phalanges is prolonged in digits II and III. Histology showed that the apical ectoderm was thickened into a cap. There was a weak ridge‐like structure in some embryos. The cap or ridge formed part of a bud‐like mass that persisted on digits II and III at stages when it had disappeared from other digits. Thus the dolphin differs from other mammals in showing a second period of limb outgrowth during which localized hyperphalangy develops. New phalanges only formed at the tip of the digits. These findings are consistent with a model in which heterochrony leads to the terminal addition of new phalanges. Our results are more easily reconciled with the progress zone model than one in which the AER is involved in the expansion of a prepattern. We suggest that patterning mechanisms with a temporal component (i.e., the “progress zone” mechanism) are potential targets for heterochrony during limb evolution.

Evolutionary Morphology and Acoustics in the Dolphin Skull

Cetaceans are the most fascinating creatures in the animal kingdom. They adapted so perfectly to their aquatic habitat that it is hard to imagine they originated from typical tetrapod land mammals. Naturally, this change to an extremely different habitat brought about profound modifications and specializations in the cetacean sensory world. Dolphins have a fairly effective visual system, which allows good sight above and below the water surface (Nachtigall, 1986; Dral, 1987). The peripheral olfactory system is reduced totally, but still occurs during early ontogenesis (Jacobs et al., 1971; Oelschlager and Buhl, 1985a, b) while the taste organ, in principle, is retained (Nachtigall and Hall, 1984). Cutaneous sensitivity seems to be fairly good in cetaceans (Herman and Tavolga, 1980) and there are indications that dolphins may possess a magnetic sense (Zoeger et al., 1981; Bauer et al., 1985; Kirschvink et al., 1986; Credle, 1988). However, it is the acoustic system, which is clearly dominant and optimized by a highly efficient ultrasound transmitter for echolocation. The latter may be connected functionally with the unusually well-developed terminalis system (Demski et al., 1985; Buhl and Oelschlager, 1986; Oelschlager et al., 1987; Ridgway et al., 1987; Oelschlager, 1989). Some toothed whales presumably can...,“emit sounds so intense that their prey is debilitated and capture made easier” (Norris and Mohl, 1983).

Quantitative neuroanatomy of the brain of the La Plata dolphin, Pontoporia blainvillei

SummaryThe brain of the La Plata dolphin, Pontoporia blainvillei, was studied with methods of quantitative morphology. The volumes and the progression indices of the main brain structures were determined and compared with corresponding data of other Cetacea, Insectivora and Primates.In Pontoporia, encephalization and neocorticalization are clearly greater than in primitive (“basal”) Insectivora. The indices are in the lower part of the range for simian monkeys. The paleocortex is regressive in accordance with the total reduction of the olfactory bulb and olfactory tract. In contrast to the situation in primates, the septum, schizocortex and archicortex are not progressive in Pontoporia. The striatum and cerebellum are strongly progressive, corresponding to the efficiency and importance of the motor system in the three-dimensional habitat. The diencephalon, mesencephalon and medulla oblongata show considerable progression. Obviously, this is correlated with the extensive development of structures of the acoustic system.The superficial correspondence of the brains of dolphins and primates in relative size and in the degree of gyrencephaly is rather a rough morphological convergence than a sign of functional equivalence. It is coupled to a strongly divergent development of the various functional systems in the two mammalian orders according to their specific evolution.

Ontogenesis of the sperm whale brain

The development of the sperm whale brain (Physeter macrocephalus) was investigated in 12 embryos and early fetuses to obtain a better understanding of the morphological and physiological adaptations in this most exotic cetacean concerning locomotion, deep diving, and orientation. In male adult sperm whales, the average absolute brain mass and the relative size of the telencephalic hemisphere are the largest within the mammalia, whereas the ratio of the brain mass to the total body mass is one of the smallest.

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.

Functional morphology of the nasal complex in the Harbor Porpoise (Phocoena phocoena L.)

Toothed whales (Odontoceti, Cetacea) are the only aquatic mammals known to echolocate, and probably all of them are able to produce click sounds and to synthesize their echoes into a three‐dimensional “acoustic image” of their environment. In contrast to other mammals, toothed whales generate their vocalizations (i.e., echolocation clicks) by a pneumatically‐driven process in their nasal complex. This study is dedicated to a better understanding of sound generation and emission in toothed whales based on morphological documentation and bioacoustic interpretation. We present an extensive description of the nasal morphology including the nasal muscles in the harbor porpoise (Phocoena phocoena) using macroscopical dissections, computer‐assisted tomography, magnetic resonance imaging, and histological sections. In general, the morphological data presented here substantiate and extend the unified “phonic lips” hypothesis of sound generation in toothed whales suggested by Cranford et al. (J Morphol 1996;228:223–285). There are, however, some morphological peculiarities in the porpoise nasal complex which might help explain the typical polycyclic structure of the clicks emitted. We hypothesize that the tough connective tissue capsule (porpoise capsule) surrounding the sound generating apparatus is a structural prerequisite for the production of these high‐frequency clicks. The topography of the deep rostral nasal air sacs (anterior nasofrontal and premaxillary sacs), narrowing the potential acoustic pathway from the phonic lips to the melon (a large fat body in front of the nasal passage), and the surrounding musculature should be crucial factors in the formation of focused narrow‐banded sound beams in the harbor porpoise. Anat Rec, 292:902–920, 2009.

Morphology and Evolutionary Biology of the Dolphin (Delphinus sp.) Brain – MR Imaging and Conventional Histology

Whole brains of the common dolphin (Delphinus delphis) were studied using magnetic resonance imaging (MRI) in parallel with conventional histology. One formalin-fixed brain was documented with a Siemens Trio Magnetic Resonance scanner and compared to three other brains which were embedded in celloidin, sectioned in the three main planes and stained for cells and fibers. The brain of the common dolphin is large, with the telencephalic hemispheres dominating the brain stem. The neocortex is voluminous and the cortical grey matter thin but extremely extended and densely convoluted. There is no olfactory ventricular recess due to the lack of an anterior olfactory system (olfactory bulb and peduncle). No occipital lobe of the telencephalic hemisphere and no posterior horn of the lateral ventricle are present. A pineal organ could not be detected. The brain stem is thick and underlies a very large cerebellum. The hippocampus and mammillary body are small and the fornix is thin; in contrast, the amygdaloid complex is large and the cortex of the limbic lobe is extended. The visual system is well developed but exceeded by the robust auditory system; for example, the inferior colliculus is several times larger than the superior colliculus. Other impressive structures in the brainstem are the peculiar elliptic nucleus, inferior olive, and in the cerebellum the huge paraflocculus and the very large posterior interpositus nucleus. There is good correspondence between MR scans and histological sections. Most of the brain characteristics can be interpreted as morphological correlates to the successful expansion of this species in the marine environment, which was characterized by the development of a powerful sonar system for localization, communication, and acousticomotor navigation.

Ontogenetic development of the nervus terminalis in toothed whales

SummaryFor 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.

The dolphin brain—A challenge for synthetic neurobiology

Toothed whales (odontocetes) are a promising paradigm for neurobiology and evolutionary biology. The ecophysiological implications and structural adaptations of their brain seem to reflect the necessity of effective underwater hearing for echolocation (sonar), navigation, and communication. However, not all components of the auditory system are equally well developed. Other sensory systems are more or less strongly reduced such as the olfactory system and, as an exception among vertebrates, the vestibular system (the semicircular canals and vestibular nuclei). Additional outstanding features are: (1) the hypertrophy of the neocortex, pons, cerebellum (particularly the paraflocculus), the elliptic nucleus, the facial motor nucleus and the medial accessory inferior olive and (2) the reduction of the hippocampus. The screening of brain structures with respect to shared circuitry and shared size correlations resulted in central loops also known from other mammals which overlap in the cerebellum and serve in the integration and processing of sensory input. It is highly probable that for dolphin navigation the ascending auditory pathway, including the inferior colliculus and the medial geniculate body, is of utmost importance. The extended auditory neocortical fields project to the midbrain and rhombencephalon and may influence premotor and motor areas in such a way as to allow the smooth regulation of sound-induced and sound-controlled locomotor activity as well as sophisticated phonation. This sonar-guided acousticomotor system for navigation and vocalization in the aquatic environment may have been a major factor if not the key feature in the relative size increase seen in dolphin brains.