Microvascular characteristics of the acoustic fats: Novel data suggesting taxonomic differences between deep and shallow‐diving odontocetes

Abstract

Odontocetes have specialized mandibular fats, the extramandibular (EMFB) and intramandibular fat bodies (IMFB), which function as acoustic organs, receiving and channeling sound to the ear during hearing and echolocation. Recent strandings of beaked whales suggest that these fat bodies are susceptible to nitrogen (N ) gas embolism and empirical evidence has shown that the N solubility of these fat bodies is higher than that of blubber. Since N gas will diffuse from blood into tissue at any blood/tissue interface and potentially form gas bubbles upon decompression, it is imperative to understand the extent of microvascularity in these specialized acoustic fats so that risk of embolism formation when diving can be estimated. Microvascular density was determined in the EMFB, IMFB, and blubber from 11 species representing three odontocete families. In all cases, the acoustic tissues had less (typically 1/3 to 1/2) microvasculature than did blubber, suggesting that capillary density in the acoustic tissues may be more constrained than in the blubber. However, even within these constraints there were clear phylogenetic differences. Ziphiid (Mesoplodon and Ziphius, 0.9 ± 0.4% and 0.7 ± 0.3% for EMFB and IMFB, respectively) and Kogiid families (1.2 ± 0.2% and 1.0 ± 0.01% for EMFB and IMFB, respectively) had significantly lower mean microvascular densities in the acoustic fats compared to the Delphinid species (Tursiops, Grampus, Stenella, and Globicephala, 1.3 ± 0.3% and 1.3 ± 0.3% for EMFB and IMFB, respectively). Overall, deep-diving beaked whales had less microvascularity in both mandibular fats and blubber compared to the shallow-diving Delphinids, which might suggest that there are differences in the N dynamics associated with diving regime, phylogeny, and tissue type. These novel data should be incorporated into diving physiology models to further understand potential functional disruption of the acoustic tissues due to changes in normal diving behavior.

Variation in the endogenous intact waxes of odontocetes: There is more than one way to build an acoustic receiver

“…In addition to the effects of the structure, distribution, and concentration of lipid molecules on sound focusing, some animals alter blood flow through the tissues to change the phase of the lipids, further affecting sound properties (Houser et al, 2004). The acoustic fat bodies have varying amounts of microvasculature, with the short‐finned pilot whales having a higher degree of microvasculature in their jaw fats than pygmy sperm whales and beaked whales (Gabler et al, 2018). However, the control that these animals have over temperature and therefore lipid phase using blood flow is unknown.…”

Potential Candidate Genes and Pathways Affecting the Metabolism of Jaw Fats in Risso’s Dolphin: Based on Transcriptomics

“…However, there are no comprehensive studies recorded on the jaw fats of many toothed whales, and its functional mechanism in echolocation still not cleared. Another study 3 found a difference in the microvascular distributions in both jaw fat tissues in some species; however, these were lower when compared to the blubber fat. One possible reason for this difference is the reduction of gas exchanges and interference of sound pathways.…”

“…Acoustic fats located in the head region, commonly categorized as melon fat and mandibular/jaw fats, play a crucial role in transmitting and receiving sounds, respectively [1][2][3] . Jaw fats are present at the outer and inner regions of the lower jaw and act as a "jawphone" that hears the returning echoes 4 ; these are also accredited for directing waveguide sounds towards the ear (Aroyan et al, 1992;Koopman et al, 2006a).…”

Remarkable consistency of spinal cord microvasculature in highly adapted diving odontocetes

“…Given these observations, it is valuable to assess the potential risk of DCS within marine mammals. The work of McClelland et al (2012) , Gabler et al (2018) , and Gabler-Smith et al (2020) have demonstrated the potential for gas exchange and nitrogen embolism in some marine mammals in two tissues with high lipid content: blubber (the adipocyte-rich hypodermis covering the body) and acoustic fats (specifically, the fat bodies covering and surrounding the mandibles, associated with sound reception in echolocating odontocetes) ( Norris, 1968 ; Pond, 1998 ; Lonati et al, 2015 ). However, there is a lack of research dedicated to the spinal cord, the site of the more severe and potentially fatal Type II form of DCS.…”