Bowhead whales are harvested by Alaskan Natives (Iñupiat and Yupik), to meet their nutritional and cultural needs, in several villages along the Bering, Chukchi and Beaufort Seas under the auspices of the US Marine Mammal Protection Act, the Endangered Species Act, the NOAA/AEWC (National Oceanic and Atmospheric Administration/Alaska Eskimo Whaling Commission) Cooperative Agreement, and the US membership to the International Whaling Commission (IWC). The Department of Wildlife Management of the North Slope Borough collects data and samples from these whales with the permission of the captains, the Barrow Whaling Captains’ Association, and the AEWC, and reports to the IWC. Our samples were collected under NOAA-NMFS permit No. 17350–00 in Barrow, Alaska.

We used a microCT scanner (Scanco Viva CT 75 Scanner at 70kVp, 114μA, slice thickness of 41 μm) to study several variables, discussed below, of the bone tissue that constitutes the second rib. Larger slices were cut to fit in the scanner and the results averaged based on the proportion they make up of the whole section evaluated. The scanner determines bone density in mg hydroxyapatite per cm³ of bone by matching the profile of the sample to a standardized hydroxyapatite phantom. As such, for bone density measurements, all bone in a sample is measured and density is calculated as the mean value of all density measurements.

The images from the scanner were converted to TIFF format and transferred to Avizo 9.0 3D software where a single, cross-sectional slice was extracted (Fig 2). These TIFF images were examined in ImageJ 1.49c, an open source image processing program that was developed at the National Institute of Health. Thresholds for the images followed the isodata method of ImageJ bone analysis software, BoneJ version 1.3.11, which is integrated with ImageJ. We used ImageJ to measure the total cross-sectional areas of each CT slice (Fig 2), as well as the percentage of the total area that was taken up by bone (as opposed to soft tissue between the trabeculae). To visualize trends, we fitted local regression scatterplot smoothing curves to the results (using the loess smoother technique as described in [13]) and implemented in R (R Core Team (2014).

The life of a newborn bowhead whale is influenced by the advance and retreat of the sea ice and food availability, just like that of the rest of the stock [1–3, 10]. Birth usually takes place during the northward spring migration. After that, females nurse during the summer feeding season in the Beaufort and Chukchi Seas and may continue nursing through autumn in the Bering Sea. Calves are weaned during the late autumn and early winter ([1–3, 10], Fig 6). Yearlings have thick blubber and sub-dermal fat layers and heavy ribs during their independent northward migration. In subsequent years, blubber layers and rib mass decrease, possibly because the whale’s small baleen rack limits the amount of food that can be procured. We propose that the dense bone provides resources which are needed to build the baleen and the upper jaws in which the baleen plates are anchored. Vertebrates store calcium in their bones, and calcium is an important component of baleen [14]. Both baleen plates and skull grow after weaning, increasing the effective baleen filtering area (Fig 6 [10]), and this growth is at the expense of growth of the rest of the body. In addition to providing resources, catabolism of fat and bone in the chest would affect buoyancy in opposite ways, given that the specific density of these tissues is, respectively, lower and higher than that of water. This may provide a control mechanism for buoyancy.

It is clear that baleen plates do not grow isometrically with body size in the first decade of bowhead life. In fact, the unusual growth pattern of the bowhead head is initiated during the fetal period [15]. This leads to a vastly different body form for whales of different ages, with heads growing disproportionally larger as they age (outlines in Fig 6). The inverse trend occurs in most mammals, where the head grows with negative allometry compared to the body. Indeed, the differences in bowhead body/head proportions of different ages are so large that there was speculation that two species were represented [16]. Alaskan Iñupiat people [17] use the word ‘ingutuk’ to refer to the rotund yearlings [17] and ‘qairilik’ for thin or “tapered” whales of similar length or larger. Yankee whalers called whales that did not yield much oil ‘dry-skins’ some of which may have been qairilik [18].

Bowhead whales share portions of their arctic feeding grounds with gray whales (Eschrichtius robustus), but there is no evidence for a growth hiatus in that species [19]. But then again, gray whales have the shortest and fewest baleen plates of any mysticete [20], and this makes baleen a small investment and may allow yearlings to feed as effectively as adults.

The sister group to bowhead whales are the right whales (Eubalaena) which live in temperate and sub-arctic waters. These whales also show a slow-down in body growth and a decrease in blubber thickness in the years immediately after weaning [21–23]. Right whale baleen growth rates are faster than those of bowhead, but the pattern of slowdown of growth with age is similar [6, 21].

Severe bone loss early in life is very unusual in mammals [24]. In otherwise healthy humans, bone loss can be the result of extreme exercise [25], but also of starvation [26]. In our model, such bone loss is normal in the early stages of a bowhead’s life as baleen and skull grow in order to increase feeding efficiency. Few mammals exploit existing bones to make new bone in a different anatomical region to the extent that bowheads do. Perhaps the best comparison to the bowhead example is found in male cervids, in which the high growth rate of antlers causes temporary physiological osteoporosis [27,28]. Similar to bowhead, bone loss in cervids occurs specifically in non-loaded parts of the skeleton [29], including ribs [30].

Marine vertebrates commonly use bone to control buoyancy [31–34], and the genetic context of some of these adaptations is understood [35]. Changes of bone density with ontogeny occur in plesiosaurs where adults are not pachyosteosclerotic while juveniles are [36]. Among cetaceans, variations in hypo- and hyperostosis have been documented in Eocene species. Such patterns are linked to hunting techniques: fast predators had light bones, whereas ambush predators and bottom walkers had heavy bones [36–40]. In these fossil whales, ribs have been shown to be liable to change, often with dorsal and ventral parts being different morphologically [39–41], reminiscent of the bowhead pattern. The inability of bowheads to obtain sufficient resources for growth may be due to ineffective feeding caused by slow growth of the baleen. This could be the main driver of blubber and bone loss in bowhead. However, the fossil whales studied have teeth, not baleen, and most authors suggest that buoyancy control is the critical factor in their bone loss patterns.