Ontogeny and evolution of the sound-generating structures in the infraorder Delphinida (Odontoceti: Delphinida)

Abstract

The ontogeny of the structures involved in sound generation and modulation in dolphins was investigated through a comparison of the soft nasal structures of foetal, perinatal, neonatal and adult specimens of Pontoporiidae, Phocoenidae and Delphinidae. Foetal samples were sectioned at 10 µm in the saggital and coronal planes, and stained for histological examination. Computed tomography and magentic resonance imaging scan series were combined with new data to represent the ontogenetic stages of the three groups. The images were analysed in 3D-Slicer to characterize the general head topography. The origins of the melon and the vestibular air sac were detected between Carnegie stages C16 and F22. The three groups analysed showed distinct formation of the nasal plug and nasal plug muscles, mainly with regard to the loss of fat pathways (or their maintenance in Pontoporiidae) and the development of the nasal plug muscles on both sides (during perinatal development of Phocoenidae) or just on the left side (during postnatal development in Delphinidae). Broadband vocalizing delphinidans might have evolved under heterochronic events acting on the formation of sound-generating structures such as the rostrum and vestibular air sacs, and on the transformation of the branches of the melon, probably leading to a reduced directionality of the sonar beam.

Head adaptation for sound production and feeding strategy in dolphins (Odontoceti: Delphinida)

“…Most dolphins of the infraorder Delphinida, particularly delphinids, produce broadband sounds (BB) for echolocation (Au, 2000). However, some lineages have independently evolved the ability to produce highly directional (Wei et al, 2019) narrow-band high frequency (NBHF) sounds (Kyhn et al, 2010) has revealed that species with highly directional signals convergently developed distinct head features to achieve increased directionality (Frainer et al, 2019a). However, feeding strategy might also determine sound emission patterns as not only preferred preys might differ between strategies (McCurry et al, 2017), but emitted sounds may also be affected by distinct rostrum morphologies adapted for suction or raptorial feeding (Song et al, 2016;Werth, 2006).…”

Blowhole anomaly in pantropical spotted dolphin (Delphinidae: Stenella attenuata)

“…The vestibular, accessory, and premaxillary sacs are relatively conservative in the delphinids, with the nasofrontal sac being the most variable portion of the system (Heyning & Mead, 1990). The hypothesis of an ontogenetic anomaly since fetal development should not be discarded, as the development of the respiratory apparatus and sound‐generating structures from delphinids starts during fetal phases (Frainer et al, 2019). Late stages of the fetal development, particularly Carnegies stages C18 to F22, are important for tissue formation around the blowhole of delphinids (Frainer et al, 2019).…”

“…The hypothesis of an ontogenetic anomaly since fetal development should not be discarded, as the development of the respiratory apparatus and sound‐generating structures from delphinids starts during fetal phases (Frainer et al, 2019). Late stages of the fetal development, particularly Carnegies stages C18 to F22, are important for tissue formation around the blowhole of delphinids (Frainer et al, 2019). In this context, an opening of a second blowhole after full development of that apparatus would likely undermine its functionality (Frainer et al, 2019).…”

“…Late stages of the fetal development, particularly Carnegies stages C18 to F22, are important for tissue formation around the blowhole of delphinids (Frainer et al, 2019). In this context, an opening of a second blowhole after full development of that apparatus would likely undermine its functionality (Frainer et al, 2019).…”

Determinants of echolocation click frequency characteristics in small toothed whales: recent advances from anatomical information

“…Therefore, soft tissue morphology is likely to be important in the frequency‐determining mechanism, as the acoustic properties of clicks may be influenced by the morphology of the soft tissues of the sound‐producing organs (Cranford et al 1996, Aroyan et al 2000). Interspecific differences in the melon terminal branch (Amundin 1991, Cranford et al 1996, Frainer et al 2019) and the dense connective tissue that covers the posterior end of the melon observed in Phocoenidae, called the ‘porpoise capsule’ (Huggenberger et al 2009), might be involved in the click frequency‐determining mechanism. In addition, vestibular sacs with many plicae (folds), observed in Phocoena phocoena , Phocoenoides dalli , and Neophocoena phocaenoides , are considered to be involved in the generation of NBHF clicks (Curry 1992, Nakamura 1999).…”