Stefan Huggenberger

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.

Head morphology in perinatal dolphins: a window into phylogeny and ontogeny.

In this paper on the ontogenesis and evolutionary biology of odontocete cetaceans (toothed whales), we investigate the head morphology of three perinatal pantropical spotted dolphins (Stenella attenuata) with the following methods: computer‐assisted tomography, magnetic resonance imaging, conventional X‐ray imaging, cryo‐sectioning as well as gross dissection. Comparison of these anatomical methods reveals that for a complete structural analysis, a combination of modern imaging techniques and conventional morphological methods is needed. In addition to the perinatal dolphins, we include series of microslides of fetal odontocetes (S. attenuata, common dolphin Delphinus delphis, narwhal Monodon monoceros). In contrast to other mammals, newborn cetaceans represent an extremely precocial state of development correlated to the fact that they have to swim and surface immediately after birth. Accordingly, the morphology of the perinatal dolphin head is very similar to that of the adult. Comparison with early fetal stages of dolphins shows that the ontogenetic change from the general mammalian bauplan to cetacean organization was characterized by profound morphological transformations of the relevant organ systems and roughly seems to parallel the phylogenetic transition from terrestrial ancestors to modern odontocetes. J. Morphol., 2006.

Geographical variation in harbour porpoise (Phocoena phocoena) skulls: Support for a separate non-migratory population in the Baltic proper

Abstract We measured metric and scored non-metric characters of 242 harbour porpoise (Phocoena phocoena) skulls from the North and the Baltic Sea and subdivided them into three geographical areas: The German Bight, the outer part or transition area of the Baltic Sea (Skagerrak, Kattegat, Belt Seas, Øresund, Kiel Bight, Lübeck Bight, and Fehmarn Belt Sea), and the central Baltic Sea (Arkona Sea and waters off the eastern Swedish coast). A comparison of the skull characters by means of ANOVA, Discriminant Analysis and X2-tests revealed significant differences between the porpoises of all three areas. The results of this study indicate the existence of populations in the Baltic different from the North Sea populations. Further, we found differences between the animals from the transition area and the central Baltic Sea respectively, indicating the occurrence of a separate population in the Baltic proper. We offer a non-migratory scenario as an explanation for the central Baltic stock of the harbour porpoise based on a review of hydrographical conditions and prey species availability.

Functional Morphology of the Hyolaryngeal Complex of the Harbor Porpoise (Phocoena phocoena): Implications for its Role in Sound Production and Respiration

In several publications, it was shown that echolocation sound generation in the nasal (epicranial) complex of toothed whales (Odontoceti) is pneumatically driven. Modern hypotheses consider the larynx and its surrounding musculature to produce the initial air pressure: (a) contraction of the strong pipelike palatopharyngeal sphincter muscle complex, which connects the choanae with the epiglottic spout of the larynx, should provide much of the power for this process and (b) muscles suspending the larynx/hyoid complex from the skull base and the mandibles may support these pistonlike laryngeal movements. Here, we describe the morphology and topography of the larynx, the hyoid apparatus, and the relevant musculature in the harbor porpoise (Phocoena phocoena) with respect to odontocete vocalization and respiration. We demonstrate that the hyoid apparatus, reminiscent of a “swinging cage,” may not only be a stable framework in which the larynx can move but should support laryngeal actions by its own movements. Rostrocaudal relocations of the hyoid apparatus may thus support pistonlike actions of the larynx creating air flow into the nasal complex for sound production. The lift of the hyoid apparatus with the thick larynx in the direction of the skull base may squeeze the pharynx in the region of the piriform recesses and thus help to secure the (waterproof) tracheochoanal connection during respiration when the palatopharyngeal sphincter cannot be contracted maximally, because the air passage must remain open at the epiglottic spout. Anat Rec, 291:1262–1270, 2008.

Interlaminar Differences of Intrinsic Properties of Pyramidal Neurons in the Auditory Cortex of Mice

Cortical information processing depends crucially upon intrinsic neuronal properties modulating a given synaptic input, in addition to integration of excitatory and inhibitory inputs. These intrinsic mechanisms are poorly understood in sensory cortex areas. We therefore investigated neuronal properties in slices of the auditory cortex (AC) of normal hearing mice using whole-cell patch-clamp recordings of pyramidal neurons in layers II/III, IV, V, and VI in the current- and voltage clamp mode. A total of 234 pyramidal neurons were included in the analysis revealing distinct laminar differences. Regular spiking (RS) neurons in layer II/III have significantly lower resting membrane potential, higher threshold for action potential generation, and larger K(ir) and Ih amplitudes compared with layer V and VI RS neurons. These currents could improve temporal resolution in the upper layers of the AC. Additionally, the presence of a T-type Ca2+ current could be an important factor of RS neurons in these upper layers to amplify temporally closely correlated inputs. Compared with upper layers, lower layers (V and VI) exhibit a higher relative abundance of intrinsic bursting neurons. These neurons may provide layer-specific transfer functions for interlaminar, intercortical, and corticofugal information processing.

The size and complexity of dolphin brains—a paradox?

Dolphin brain size with respect to body size ranks between that of apes and humans. The hypertrophic auditory structures, the large cerebrum with extended gyrification and the highly cognitive capabilities of toothed whales seem to be in paradoxical contrast to their thin neocortex with a plesiomorphic or paedomorphic cytoarchitecture. The total number of neurons in the delphinid neocortex is comparable to that of the chimpanzee (Primates), but, in relation to body weight, in the magnitude of the hedgehog (Insectivora) neocortex since cetaceans may be able to obtain larger body sizes than terrestrial mammals due to reduced gravitational effects in water. During evolution, dolphins may have increased the computational performance of their cytoarchitectonically ‘simple’ neocortex by a multiplication of relevant structures (resulting in a hypertrophic surface area) instead of increasing its complexity. Based on this hypothesis, I suggest that the evolution of the large dolphin brain was possible due to a combination of different prerequisites based on adaptations to the aquatic environment including the sonar system. The latter facilitated a successful feeding strategy to support an increased metabolic turnover of the brain and led to a hypertrophic auditory system. Moreover, the rudimentary pelvic girdle did not limit brain size at birth. These adaptations favoured the evolutionary size increase of the cerebral cortex in dolphins facilitating highly cognitive capabilities as well as precise and rapid sound processing using a ‘simple’ kind of neocortical cytoarchitecture.

Histological and ultrastructural aspects of the nasal complex in the harbour porpoise, Phocoena phocoena

During the evolution of odontocetes, the nasal complex was modified into a complicated system of passages and diverticulae. It is generally accepted that these are essential structures for nasal sound production. However, the mechanism of sound generation and the functional significance of the epicranial nasal complex are not fully understood. We have studied the epicranial structures of harbor porpoises (Phocoena phocoena) using light and electron microscopy with special consideration of the nasal diverticulae, the phonic lips and dorsal bursae, the proposed center of nasal sound generation. The lining of the epicranial respiratory tract with associated diverticulae is consistently composed of a stratified squamous epithelium with incomplete keratinization and irregular pigmentation. It consists of a stratum basale and a stratum spinosum that transforms apically into a stratum externum. The epithelium of the phonic lips comprises 70–80 layers of extremely flattened cells, i.e., four times more layers than in the remaining epicranial air spaces. This alignment and the increased number of desmosomes surrounding each cell indicate a conspicuous rigid quality of the epithelium. The area surrounding the phonic lips and adjacent fat bodies exhibits a high density of mechanoreceptors, possibly perceiving pressure differentials and vibrations. Mechanoreceptors with few layers and with perineural capsules directly subepithelial of the phonic lips can be distinguished from larger, multi‐layered mechanoreceptors without perineural capsules in the periphery of the dorsal bursae. A blade‐like elastin body at the caudal wall of the epicranial respiratory tract may act as antagonist of the musculature that moves the blowhole ligament. Bursal cartilages exist in the developmental stages from fetus through juvenile and could not be verified in adults. These histological results support the hypothesis of nasal sound generation for the harbor porpoise and display specific adaptations of the echolocating system in this species. J. Morphol. 2009.

Precocious Ossification of the Tympanoperiotic Bone in Fetal and Newborn Dolphins: An Evolutionary Adaptation to the Aquatic Environment?

The present study, performed with a dual‐energy X‐ray (DXA) bone densitometer on a series of fetal and newborn striped and short‐beaked common dolphins, shows that the bone density of the area of the tympanic bulla within the tympanoperiotic complex starts with 0.483 g cm−2 in 5‐ to 6‐month‐old specimens of striped (or common) dolphin fetuses and reaches 1.841 g cm−2 in newborn striped dolphins, with values consistently higher than in other parts of the skull or elsewhere in the skeleton. The same results apply to the common bottlenose dolphins, in which the area of the tympanic bulla has a density of 0.312 g cm−2 in 5‐month‐old specimens and becomes four times as much in newborns. Regardless of the areal bone density results correlated to the DXA‐technique, comparisons with DXA‐bone density data in the literature referred to other mammals emphasize the presence of very high mineral deposition in the area of the tympanoperiotic bone in fetal and newborn dolphins and the most dense part of it belongs to the tympanic bulla. The early osseous maturation of the tympanic bulla area may be compared to what described in fin whales and may represent an unique ontogenetic and phylogenetic feature of cetaceans, possibly related to the development of essential acoustic sense and establishment of immediate post‐natal mother–calf relationship. Anat Rec, 298:1294–1300, 2015.

The dolphin cochlear nucleus: Topography, histology and functional implications

Despite the outstanding auditory capabilities of dolphins, there is only limited information available on the cytology of the auditory brain stem nuclei in these animals. Here, we investigated the cochlear nuclei (CN) of five brains of common dolphins (Delphinus delphis) and La Plata dolphins (Pontoporia blainvillei) using cell and fiber stain microslide series representing the three main anatomical planes. In general, the CN in dolphins comprise the same set of subnuclei as in other mammals. However, the volume ratio of the dorsal cochlear nucleus (DCN) in relation to the ventral cochlear nucleus (VCN) of dolphins represents a minimum among the mammals examined so far. Because, for example, in cats the DCN is necessary for reflexive orientation of the head and pinnae towards a sound source, the massive restrictions in head movability in dolphins and the absence of outer ears may be correlated with the reduction of the DCN. Moreover, the same set of main neuron types were found in the dolphin CN as in other mammals, including octopus and multipolar cells. Because the latter two types of neurons are thought to be involved in the recognition of complex sounds, including speech, we suggest that, in dolphins, they may be involved in the processing of their communication signals. Comparison of the toothed whale species studied here revealed that large spherical cells were present in the La Plata dolphin but absent in the common dolphin. These neurons are known to be engaged in the processing of low‐frequency sounds in terrestrial mammals. Accordingly, in the common dolphin, the absence of large spherical cells seems to be correlated with a shift of its auditory spectrum into the high‐frequency range above 20 kHz. The existence of large spherical cells in the VCN of the La Plata dolphin, however, is enigmatic asthis species uses frequencies around 130 kHz. J. Morphol. 2011.

Diving: Breathing, Respiration, and the Circulatory System

We may imagine dolphins as continuous breath-holding divers or marathon swimmers that continuously exercise. However, just by admitting this simple comparison, we immediately come out with a number of questions that has been difficult to answer: What about the energy required to move uninterruptedly in and out of the water surface? What about the oxygen stores required to perform prolonged breath-hold dives? What about heartbeat or breathing frequency, diaphragm movements, and the effects of external pressure? Some of these complex aspects of diving physiology are still partially unsolved in dolphins, and are outside the scope of the present book.