Brown adipose tissue in cetacean blubber.

Osamu Hashimoto,Hirofumi Ohtsuki,Makoto Sugiyama,Sara Kobayashi,Takashi Matsuishi,Hideki Endo,Takehiko Kakizaki,Kento Amou,Fumio Terasawa,Satoru Doi,Ryo Sato,Masayuki Funaba,Junji Shindo,Ayaka Matsuda,Wayne Iwan Lee Davies

doi:10.1371/journal.pone.0116734

Abstract

Brown adipose tissue (BAT) plays an important role in thermoregulation in species living in cold environments, given heat can be generated from its chemical energy reserves. Here we investigate the existence of BAT in blubber in four species of delphinoid cetacean, the Pacific white-sided and bottlenose dolphins, Lagenorhynchus obliquidens and Tursiops truncates, and Dall’s and harbour porpoises, Phocoenoides dalli and Phocoena phocoena. Histology revealed adipocytes with small unilocular fat droplets and a large eosinophilic cytoplasm intermingled with connective tissue in the innermost layers of blubber. Chemistry revealed a brown adipocyte-specific mitochondrial protein, uncoupling protein 1 (UCP1), within these same adipocytes, but not those distributed elsewhere throughout the blubber. Western blot analysis of extracts from the inner blubber layer confirmed that the immunohistochemical positive reaction was specific to UCP1 and that this adipose tissue was BAT. To better understand the distribution of BAT throughout the entire cetacean body, cadavers were subjected to computed tomography (CT) scanning. Resulting imagery, coupled with histological corroboration of fine tissue structure, revealed adipocytes intermingled with connective tissue in the lowest layer of blubber were distributed within a thin, highly dense layer that extended the length of the body, with the exception of the rostrum, fin and fluke regions. As such, we describe BAT effectively enveloping the cetacean body. Our results suggest that delphinoid blubber could serve a role additional to those frequently attributed to it: simple insulation blanket, energy storage, hydrodynamic streamlining or contributor to positive buoyancy. We believe delphinoid BAT might also function like an electric blanket, enabling animals to frequent waters cooler than blubber as an insulator alone might otherwise allow an animal to withstand, or allow animals to maintain body temperature in cool waters during sustained periods of physical inactivity.

Highlights

Despite having been first recognized in the mid-16th century [1], only over the past 50 years have the origin and function of brown adipose tissue (BAT) in mammals been subject to intensive investigative research [2]
Immunohistochemical analysis using anti-uncoupling protein 1 (UCP1) antibody revealed a concentration of brown adipocytes with a small fat droplet and large cytoplasm in the inner layer of blubber (Fig. 2); UCP1-positive cells were not observed in other blubber layers (Fig. 2)
Immunoreactivity of UCP1 in the innermost blubber layer varied between specimens (Tables 2–4), possibly because of differences in sample freshness

Summary

Introduction

Despite having been first recognized in the mid-16th century [1], only over the past 50 years have the origin and function of brown adipose tissue (BAT) in mammals been subject to intensive investigative research [2]. BAT is abundant in hibernating animals, such as small rodents, where it is concentrated in small deposits in interand subscapular, axillary, perirenal and periaortic regions of the body [2]. It has not been recorded in cetaceans, such as whales, dolphins and porpoises, of which the latter two are hereafter referred to as delphinoids (superfamily Delphinoidea). The uncoupling occurs through expression of uncoupling protein 1 (UCP1), a brown adipocyte-specific mitochondrial protein, that promotes proton leak across the inner mitochondrial membrane in mammals [3]

Methods

Results

Conclusion