Structure of the integument of southern right whales, Eubalaena australis

Authors


Abstract

Skin (integument) anatomy reflects adaptations to particular environments. It is hypothesized that cetacean (whale) integument will show unique anatomical adaptations to an aquatic environment, particularly regarding differences in temperature, density, and pressure. In this study, the gross and histological structure of the southern right whale integument is described and compared with terrestrial mammals and previous descriptions of mysticete (baleen whale) and odontocete (toothed whale) species. Samples were taken of the integument of 98 free-swimming southern right whales, Eubalaena australis, and examined by both light and electron microscopy. Results show that three epidermal layers are present, with the stratum corneum being parakeratotic in nature. As in bowhead whales, southern right whales possess an acanthotic epidermis and a notably thick hypodermis, with epidermal rods and extensive papillomatosis. However, unlike bowhead whales, southern right whales possess an uninterrupted hypodermal layer. Surprisingly, the integument of balaenids (right and bowhead mysticetes) in general is more like that of odontocetes than that of the more closely related balaenopterids (rorqual mysticetes). Similarities to odontocetes were found specifically in the collagen fibers in a fat-free zone of the reticular dermal layer and the elastic fibers in the dermal and hypodermal layers. Callosities, a distinctive feature of this genus, have a slightly thicker stratum corneum and are usually associated with hairs that have innervated and vascularized follicles. These hairs may function as vibrissae, thus aiding in aquatic foraging by allowing rapid detection of changes in prey density. Although the thick insulatory integument makes right whales bulky and slow-moving, it is an adaptation for living in cold water. Epidermal thickness, presence of epidermal rods, and callosities may act as barriers against mechanical injury from bodily contact with conspecifics or hard surfaces in the environment (e.g., rocks, ice). Anat Rec, 290:596–613, 2007. © 2007 Wiley-Liss, Inc.

The integument, or skin, of an organism is multifunctional: protecting the organism from injury, assisting in the maintenance of homeostasis, enhancing or forming locomotory devices, and displaying patterns or secreting substances that camouflage, attract, or repel. In some species, the skin is involved in fashioning certain ornamental structures (Montagna, 1967).

In all mammals, the skin forms a continuous external covering, varying in thickness, color, and distribution of epidermal appendages, such as hairs and glands in different regions of the body. The external surface layer is a keratinized stratified squamous epithelium called the epidermis. This overlies the dermis, a thick layer of dense, fibroelastic connective tissue that is highly vascular and contains many sensory receptors. The dermis is attached to underlying tissues by a layer of loose connective tissue called the hypodermis, which contains variable amounts of adipose tissue (Wheater et al., 1979).

The specific features of the skin reflect adaptations to the particular environment in which the animal lives. When compared with the terrestrial environment, the marine environment is 800 times denser, approximately 40 times more viscous, has a greater heat capacity (between 18 and 27 times that of air), and exerts greater pressure, with a 1 atmosphere increase for every 10 meters submergence below the surface. It is expressly the higher density, greater heat capacity, and greatly fluctuating pressure that determine the structure and function of the cetacean integument (Ling, 1974; Yablokov et al., 1974).

To minimize frictional resistance and maximize body streamlining, cetaceans exhibit smooth skin surfaces (e.g., see Fish et al., 2007, this issue) and typically lack hair, although there are individual vibrissae on the heads of mysticetes. Sebaceous and sweat glands are absent, and the epidermis and hypodermis are prominent (Parry, 1949; Yablokov et al., 1974; Sokolov, 1982). The skin has been described as “glabrous” or “smooth,” although superficial cutaneous ridges or furrows have been described for some species (Giacometti, 1967; Geraci et al., 1986; Shoemaker and Ridgway, 1991) that possibly play a role in tactile sensing or in improving the hydrodynamic characteristics of the animal or both (Shoemaker and Ridgway, 1991).

The histological structure of cetacean skin is significantly different in many ways from that of other mammals (Sokolov and Kalashnikova, 1971). The epidermis consists of three strata, compared with five strata in most terrestrial mammals. The outermost stratum has been referred to as the stratum corneum or the stratum externum, histochemically shown to contain keratin (Kleinenberg et al., 1964; Palmer and Weddell, 1964; Sokolov and Kalashnikova, 1971; Spearman, 1972; Simpson and Gardner, 1972; Ling, 1974; Greenwood et al., 1974; Haldiman et al., 1985; Haldiman and Tarpley, 1993), although the process of keratinization is incomplete (Harrison and Thurley, 1974; Albert et al., 1980; Migaki, 1981; Geraci et al., 1986; St. Aubin et al., 1990). Underlying the stratum corneum is the stratum spinosum (or prickle cell layer), although Harrison and Thurley (1974) subdivide the cells of this region into a lower stratum spinosum and an upper stratum intermedium, terms also used interchangeably by Geraci et al. (1986) to describe this layer. The innermost stratum of the epidermis is the stratum basale or stratum germinativum (Parry, 1949; Sokolov and Kalashnikova, 1971; Harrison and Thurley, 1974; Ling, 1974; Hicks et al., 1985). Ling (1974) also refers to this innermost stratum as the Malpighian layer. The stratum granulosum and stratum lucidum found in most other mammals appear to be absent in cetaceans. Here, the epidermal layers will be referred to the stratum corneum, spinosum, and basale, respectively, in accordance with the Nomina Histologica (1980).

A notable feature of the cetacean integument is that the epidermis is anchored to the underlying dermal connective tissue by uniformly long, moderately thick downward extensions called rete pegs or ridges, which are generally oriented parallel to the body axis. These ridges form slender flap-like projections between which dermal papillae are located (Bel'kovich, 1962; Sokolov, 1962a, b; Giacometti, 1967; Simpson and Gardner, 1972; Ling, 1974; Geraci et al., 1986). The papillae in the dermal layer project into the epidermis over almost half its thickness, significantly increasing the surface area of the germinal layer of the epidermis and contributing to its exceptional thickness (Yablokov et al., 1974). The interdigitation between the epidermal ridges and dermal papillae is referred to as papillomatosis.

The dermis is a thick bed of dense white fibrous connective tissue, blood vessels, and adipose tissue (Haldiman and Tarpley, 1993), and is richly innervated (Parry, 1949; Palmer and Weddell, 1964; Giacometti, 1967; Simpson and Gardner, 1972; Haldiman et al., 1985). Collagen dominates with fairly stout bundles that are usually orientated parallel to the skin surface, although some are randomly arranged. At deeper levels the dermis becomes invaded by, and merges with, the fatty tissue of the hypodermis (Sokolov, 1962a, b).

The hypodermis or blubber of cetaceans, with its often vast accumulation of adipocytes, or fat cells, is the most distinctive feature of the integument. Superficially, it is continuous with the reticular layer of the dermis, while proximally it is separated from the panniculus carnosus by loose connective tissue (superficial fascia). The distinction between the dermis and hypodermis is not always clear, as adipocytes extend to some extent up to the dermis and heavy collagen bundles ramify throughout the blubber (Parry, 1949; Simpson and Gardner, 1972; Ackman et al., 1975; Sokolov, 1982). The hypodermis is architecturally simple: it is usually composed of adipose tissue supported by vasculature, nerves, and varying amounts of collagen fibers.

In this study, the structure of the integument of the southern right whale is described and compared with previous descriptions of other cetacean species. Both light and electron microscopy were used to examine material from neonates, calves, juveniles, and adults, much of which has been collected by biopsy from free-swimming animals. Possible seasonal changes in the shedding of superficial skin cells (i.e., exfoliation/desquamation) are examined using material from South Africa (July–November) and the Antarctic (January–February).

Definitions

The term integument here refers to the epidermal, dermal, and hypodermal layers together. The pigmented uppermost layer of the integument is referred to as the epidermis. The generally accepted definition whereby the junction (although not always marked, as discussed above) between the dermis and hypodermis is defined by an increase in adipose tissue and a decrease in connective tissue, is followed here. Blubber refers to dermal and hypodermal layers together.

The term moult, or ecdysis, is used to describe the periodic shedding of parts or all of the outer epidermal covering, which is then replaced by a new growth, as opposed to exfoliation and desquamation, which refer to the regular removal of epidermis in flakes, scale, or peel. Sloughing refers to the shedding or casting off of the outer epidermal stratum, or parts thereof, and is regarded as a synonym for moulting.

Taxonomy

Southern right whales are here considered as a distinct species, Eubalaena australis, following Rosenbaum et al. (2000) and Gaines et al. (2005).

MATERIALS AND METHODS

Sample Collection

Samples of integument (epidermis and blubber) were collected from 35 cows and 63 calves of free-swimming southern right whales, Eubalaena australis,) in August and October, 1998 and 1999, and early November 2000, using a deep core biopsy technique (Reeb and Best, 2006). Sampling localities included Walker Bay (Gansbaai), Struisbaai, De Hoop Marine Reserve, and St. Sebastian Bay, all on the south coast of Southern Africa.

Each whale was approached perpendicular to its long axis and sampled by inserting the biopsy head (on the end of a 9-m aluminum pole) into the dorsolateral surface of the whale and immediately retracting it. Once a successful biopsy attempt was made, the sample was removed from the biopsy head, placed in foil and into a labeled plastic bag, and then put into a cooler box with re-freezable ice packs. The biopsy tool heads were cleaned in 99% chloroform between samples, and the barbs reset or, if necessary, replaced. On land, the samples were measured, noting epidermal and blubber thickness. The pigmented skin was cut away from blubber samples (the cut was made on the blubber side of the intersection between the epidermis and dermis) using a sterile scalpel, and the skin was immediately placed in a separate, labeled specimen bottle containing glutaraldehyde. Skin samples were left in the glutaraldehyde for 3–6 days and were then placed in buffer (25% glutaraldehyde plus sodium dihydrogen orthophosphate, plus disodiumhydrogen orthophosphate anhydrous, plus equal part water) until analyzed.

The thickness of the integument was measured at five positions along the mid-dorsal, lateral, and mid-ventral surfaces of southern right whales that stranded from 1998 onward (Table 1) on the south coast, round the Cape Peninsula, and at Dwarskersbos and Elands Bay on the west coast of South Africa. The positions were determined by dividing the body of the whale (between the blowholes and the caudal peduncle) into five equal parts, with Position 1 being directly behind the blowholes.

Table 1. Total lengths, girths, epidermal and blubber thicknesses of southern right whale neonates stranded along the Cape coast of South Africa 1998–2000
  • a

    Positions as described in the text.

  • b

    Measurements taken just below genital aperture.

  • c

    Measurements unobtainable.

Stranding no.98/0900/1000/1299/0500/09
SexFemaleMaleMaleMaleMale
Total length (m)3.94.424.434.845.91
Girth (m)
Position 1a2.52.382.34c2.7
Position 2a2.62.942.48∼2.32.88
Position 3a3.42.762.28c2.6
Position 4a1.21.61.48c1.58
Position 5a0.80.930.78c0.99
Epidermal thickness (cm)a
Mid-dorsal position 11.20.910.9c
Mid-dorsal position 21.30.81.30.6c
Mid-dorsal position 31.30.911.3c
Mid-dorsal position 41.40.91.51.5c
Mid-dorsal position 51.31.10.80.5c
Lateral position 1c11.4c1.1
Lateral position 2c0.81.91.11.6
Lateral position 3c1.321.31.5
Lateral position 4c1.12.41.41.4
Lateral position 5c110.90.9
Mid-ventral position 1c1c2.21.3
Mid-ventral position 2c1c1.41.7
Mid-ventral position 3c1.2bcc1.4b
Mid-ventral position 41.41c1.21
Mid-ventral position 5c1c0.61.2
Blubber thickness (cm)a
Mid-dorsal position 11.74.62.53.7c
Mid-dorsal position 21.53.23.11.5c
Mid-dorsal position 32.853.53c
Mid-dorsal position 44.58.74.35.5c
Mid-dorsal position 57.310.35.67.3c
Lateral position 13.16.71.1c4.7
Lateral position 23.45.14.74.64.9
Lateral position 33.35.43.23.86.3
Lateral position 43.84.83.235.3
Lateral position 52.84.51.893.4
Mid-ventral position 137.7c5.65.3
Mid-ventral position 24.95.7c3.74.3
Mid-ventral position 355.8bcc6.4b
Mid-ventral position 46.78.7c6.78.5
Mid-ventral position 57.36.2c4.88.8

Full core samples were taken at the same positions that the measurements were taken, placed in foil and frozen at −20°C within a few hours of collection. Samples for histological analysis were subsequently fixed in 10% buffered formalin and subsamples of the pigmented skin for electron microscopic analysis were fixed in glutaraldehyde (same procedure as for biopsy samples). In most instances, the positioning of the animal prohibited the collection of samples from both the mid-dorsal and mid-ventral surfaces and in other instances the location of the animal made it impossible to take measurements and collect samples from all positions along the various surfaces. Skin samples from other structures (e.g., callosities, flippers, and flukes) were collected opportunistically (Table 2).

Table 2. Details of stranded southern right whales where integument was sampled for histological examination
Sample no.TypeDateAgeLocationTotal length (m)Gender
84/27Mid-dorsal Pos 3 or 409/08/84JuvenileGansbaai9.25?
86/32Mid-dorsal Pos 3 or 409/02/86NeonateDe Hoop4.85Male
89/30Mid-dorsal Pos 3 or 412/06/89AdultGansbaai14.7Male
90/29Mid-dorsal Pos 3 or 416/08/90NeonateHermanus4.8Female
91/18Mid-dorsal Pos 3 or 413/09/91NeonateDe Hoop6.65Male
94/12Mid-dorsal Pos 3 or 422/09/94JuvenileBreede River11.23Female
98/09Mid-dorsal Pos 1–520/08/98NeonateWitsand3.9Female
98/09Mid-ventral Pos 420/08/98NeonateWitsand3.9Female
98/09Callosity20/08/98NeonateWitsand3.9Female
99/05Mid-dorsal Pos 1–516/09/99NeonateHermanus4.84Male
99/05Right Lateral Pos 1–516/09/99NeonateHermanus4.84Male
99/05Mid-ventral Pos 1/2/4/516/09/99NeonateHermanus4.84Male
99/05Callosity16/09/99NeonateHermanus4.84Male
99/05Fluke16/09/99NeonateHermanus4.84Male
00/09Mid-dorsal Pos 324/07/00NeonateWitsand5.91Male
00/10Mid lateral Pos 229/07/00NeonateElands Bay4.42Male
00/11Left lateral Pos 1–506/09/00JuvenileSea Point9.85Female
00/11Bonnet06/09/00JuvenileSea Point9.85Female
00/12Mid-dorsal Pos 418/09/00NeonateDwarskersbos4.43Male
00/12Flipper, fluke, bonnet18/09/00NeonateDwarskersbos4.43Male
00/12Lower lip18/09/00NeonateDwarskersbos4.43Male
00/14Dorsolateral Pos 1–513/10/00SubadultCape Point15.7Male
00/14Callosity13/10/00SubadultCape Point15.7Male

Skin biopsies (n = 14, but only 11 were suitable for histological analysis) were also obtained from southern right whales in the Antarctic during the 1998/1999 IWC/SOWER Circumpolar Cruise (Table 3). Samples were collected using a crossbow, Paxarms biopsy rifle or Japanese air gun, and were exported from Japan under CITES permit number T-AG 99-100172(W). The protocol mentioned above for biopsy samples, was also followed for these samples.

Table 3. Details of free-swimming southern right whales in Antarctic watersa
Sample no.TypeDateAgeLocationLength (m)Gender
  • a

    Epidermal/dermal samples were collected for histological examination. n/a = not applicable; ud = undetermined.

29SBiopsy25/01/99Non-calf650335S/0884517En/aud
35SBiopsy26/0199Non-calf633292S/0912944En/aud
44SBiopsy29/01/99Non-calf624021S/0961232En/aud
46SBiopsy31/01/99Non-calf624012S/0992990En/aud
64SBiopsy14/02/99Non-calf622174S/1185408En/aud
140SBiopsy05/02/99Non-calf631935S/1032848En/aud
146SBiopsy09/02/99Non-calf643123S/1130600En/aud
147SBiopsy11/02/99Non-calf641172S/1171433En/aud
149SBiopsy14/02/99Non-calf641714S/1173543En/aud
150SBiopsy14/02/99Non-calf633632S/1185262En/aud
151SBiopsy14/02/99Non-calf633632S/1185262En/aud

These activities were carried out under permits issued to P.B.B. in terms of the Sea Fishery Act, 1988 (Act no. 12 of 1988), and the Marine Living Resources Act (Act no. 18 of 1998), on 10 March 1998 and 29 January 1999, respectively.

Histological Preparations

Standard protocols to determine cell proliferation activity within the germinal layers, as well as protocols for light microscopy, scanning electron microscopy, and transmission microscopy were followed.

Skin samples were prepared, paraffin-embedded, and stained according to standard histological procedures. A tissue processor (Leica Jung Histokinette 2000, Leica Microsystems Nussloch GmbH, Nussloch, Germany) was used, sections of 4–5 μm were cut on a microtome and adhered to 3-aminopropyltriethoxysilane (APES) -coated slides. Mayer's hematoxylin and eosin stains were used to accentuate general histological structure, Weigert's resourcin stain to reveal the presence of collagen and elastin fibers, and Ayoub-Shklar stain to reveal keratin.

Samples for transmission electron microscopy (TEM) were prepared in a standard manner (Bancroft and Stevens, 1990), and electron micrographs were taken using a Hitachi H600 transmission electron microscope (Hitachi High Technologies Canada, Inc., Ontario, Canada) at various magnifications, operating at 75 kV.

Samples for scanning electron microscopy (SEM) were removed from buffer and dehydrated through an ethanol (Merck AG Ethanol, Merck & Co., Inc., Whitehouse Station, NJ) series (30%, 50%, 70%, 80%, 90%, 100%) for 2.5 hours in each solution. The samples were placed in two additional washes of absolute alcohol for 2.5 hours each. The samples were critical point dried from 100% EtOH in CO2, mounted and coated with gold-palladium in a sputter coater, and viewed using a JEOL JSM-5200 scanning electron microscope (JEOL-USA, Inc., Peabody, MA) operating at 15 kV.

Statistical Analyses

The Student's t-test (for normally distributed data) and the Mann-Whitney rank sum test (SigmaStat for Windows, Jandel Scientific Software) were used to statistically compare variations in epidermal and blubber thicknesses between different positions along the whale's body and between different age groups. An alpha value of 0.05 was used.

RESULTS

General Characteristics of Southern Right Whale Skin

Although many samples were obtained from live animals, being biopsies these were restricted to random sampling of limited areas of the back. Stranded animals provided a better opportunity for more detailed examination of the integument of southern right whales. Raised areas of skin (“callosities”) occur on the rostrum and caudal to the blowholes of southern right whales (Fig. 1) and are also present in a regular row along both sides of the mandible, each side of the chin and immediately above each eye (Matthews, 1938). In stranded neonates, the callosities were smooth and lighter in color than the rest of the skin. A stiff, single hair usually emerged from the center of each of the smaller callosities, while in larger callosities (such as the “bonnet” at the tip of the rostrum), several individual hairs arose from the centers of several coalesced bumps. Associated with these structures in older calves, juveniles, and adults, were barnacles (Tubicinella sp., Fig. 2a) and small amphipod crustaceans (Cyamus sp., Fig. 2b), which gave these structures shades of white, yellow, and orange coloration. Within the larger callosities, projections of pigmented skin seemed to form “epidermal stalks,” varying in length, but generally only long enough to project a few centimeters above the surrounding tissue (Fig. 2a). According to Payne et al. (1983), these stalks may be formed when callosity tissue extends high enough to reach water that is moving too fast to be suitable habitat for cyamids, resulting in a release of grazing pressure (discussed further below). The tip of the snout and chin possess several similar hairs that are not associated with callosities: these number 15–96 (average 60) and 125–224 (average 179), respectively, in North Pacific right whales, and reach a length of 17 mm (Omura et al., 1969). In southern right whales, they are arranged as dense groupings on the snout and at the tip of each mandible, forming a rough triangle (Fig. 3).

Figure 1.

Raised areas of skin (arrows) on the rostrum and mandible of an adult southern right whale. Note white patch on the mid-dorsal surface used for individual identification.

Figure 2.

A,B: Cyamids, epidermal stalks (arrow, A) and barnacles (B) on the bonnet callosity of a southern right whale.

Figure 3.

Dense grouping of hairs on the snout, and as separate groupings at the tip of each mandible, joined by a narrow band across the chin of a southern right whale, forming a rough triangle (arrows).

The gross appearance of the general epidermal surface of noncalves was usually smooth. Fresh epidermis had a smooth, rubbery consistency, reminiscent of neoprene material. Apart from the callosities, the head and body were generally black in color, with variably sized white areas on the belly and sometimes on the back. Schaeff et al. (1999) recognize three dorsal color variants in southern right whales: those with a white blaze that remains white throughout life, those with a white mark that darkens to gray (partial-gray morphs), and those that are born predominantly white but then darken to gray (gray morphs), the last two may be sex-linked.

Discoloration of the skin surface, due to diatom films, was not seen on any animals (although this discoloration may be difficult to observe in right whales owing to their generally black coloration). The outermost layer of the epidermis (the stratum corneum) was a macroscopic, thin superficial layer of cells that separates easily from the rest of the epidermis and was continually being sloughed (at least in temperate waters). Sloughed areas gave the skin a gray-patchy look, as frequently seen in adult right whales off South Africa (Fig. 4).

Figure 4.

Gray patches (arrows) caused by sloughing of the superficial stratum corneum on the head of an adult southern right whale.

The epidermis was usually heavily pigmented, and was noticeably thick (Fig. 5). In stranded neonates it varied slightly in thickness around the body, with the average epidermal thickness along the mid-dorsal, lateral, and mid-ventral planes being 1.13 ± 0.2 cm (n = 4), 1.52 ± 0.3 cm (n = 4), and 1.14 ± 0.2 cm (n = 4), respectively (Table 1). However, when comparing these epidermal thicknesses (between the mid-dorsal, lateral, and ventral planes of stranded neonates) statistically, the thicknesses were not significantly different (P > 0.05) from each other. The mean (± S.E.) epidermal thickness of calves biopsied in August/September (1.57 ± 0.13 cm [n = 20]) did not differ from those biopsied in October/November (1.39 ± 0.07 cm [n = 19]) (P = 0.261). The corresponding adult measurements were 1.42 ± 0.09 cm (n = 13) and 1.43 ± 0.08 cm (n = 9; P = 0.934), respectively. The differences between early season calves and early season adults (P = 0.552), early season calves and late season adults (P = 0.587), late season calves and early season adults (P = 0.851), and late season calves and late season adults (P = 0.725) were not significant.

Figure 5.

A core sample taken through the integument of a neonatal southern right whale. The epidermal layers (E) are heavily pigmented and noticeably thick. Dermal layer (D), hypodermal layer (H), superficial fascia (Sf) are shown.

The dorsal epidermis of the fluke of a neonate (1 cm) was slightly thicker than the ventral epidermis (0.5 cm) (Fig. 6). The core of the flipper and fluke (Fig. 6) possessed more abundant coarse, white connective tissue strands than any other body region studied. The skin of one freshly stranded neonate had an unusual appearance. On close inspection of the skin, it seemed as if the dermal papillae were exposed and the entire epidermis was missing, lost or not yet properly formed in some regions. Histological preparations of 15 skin samples from all over the body of this neonate confirmed the presence of stratum spinosal cells, but the entire stratum corneum was absent in all but one sample (on the right mid-lateral plane), due to a pathological condition (Reeb et al., 2005a).

Figure 6.

Longitudinal section through the fluke tip of a southern right whale calf. Note the thicker dorsal epidermis (D) compared with the ventral epidermis (V) and extensive collagen fibers (F), colored light pink, ramifying through core of the fluke. (hematoxylin and eosin stain; original magnification, 8×).

Microscopic Characteristics of Southern Right Whale Skin

Superficial epidermal features.

Cutaneous ridges or furrows were absent on the epidermal surfaces of all samples and upon gross examination, the skin of adults and darkly colored calves appeared smooth and uniform in color. However, scanning electron microscopy showed flaking of the surface squamous keratinocytes (Fig. 7a) in both early and late season adults and calves, as well as in animals sampled in the Antarctic (Fig. 7b). The surface cells may desquamate individually or in sheets, with the cells showing close apposition to each other. Distinct pentagon-shaped cell junctions and deep surface ridges formed a honeycomb-like pattern resembling those of terrestrial mammals (Fig. 7c,d). The texture of the skin in areas where epidermal sloughing occurred looked uniformly pitted, exposing the disconnected and freed intercellular boundaries (Fig. 7e). Sloughing occurred in multiple layers (Fig. 7f).

Figure 7.

A: Scanning electron microscope images showing the flaking of superficial squamosal keratinocytes of a late season southern right whale calf (A, original magnification, 75×) and of an adult southern right whale sampled in Antarctic waters (B, original magnification, 100×). C,D: Superficial keratinocytes with distinct pentagonally shaped cell junctions (j) forming deep surface ridges in a honeycomb-like pattern (arrows), individual epidermal cells in the process of sloughing (C), (D) cell boundaries formed by epidermal cells that have already sloughed (D, original magnification, 750×). E: Uniformly pitted appearance of the superficial epidermis exposing the disconnected and freed intercellular boundaries (arrow), after sloughing has occurred (original magnification, 3,500×). F: Multilayered superficial epidermal moult of a subadult southern right whale (original magnification, 50×).

Differences in the macroscopic appearance of the skin of calves were noted at sampling, and they were grouped accordingly. Calves with dark, smooth-looking skin were termed “smooth-skinned,” and calves with light gray and seemingly “broken” skin were termed “rough-skinned” (Reeb et al., 2005b). The skin of early season, smooth-skinned calves possessed patches of smooth epidermis with no honeycomb patterns visible on the surface; these patterns gave way to the exposed, pitted surface of recently sloughed areas as seen in adults (Fig. 7d). The presence of randomly dispersed white/gray dots, surrounded by dark rings, was also noted on the superficial epidermis of all smooth-skinned animals (Fig. 8).

Figure 8.

“Dots” on the surface of the skin of a southern right whale sampled in the Antarctic showing the distinct dark ring (arrow) around the dots.

Rough-skinned calves did not show the typical sloughing features as described above: instead, the surface skin of these animals was uneven (Fig. 9a), with no visible dots. However, scanning electron microscopy revealed keratinocytes forming rosettes around, and superficial to, dermal papillae (Fig. 9a), which together, presumably formed the superficial dots seen on smooth-skinned animals. Rosettes were also exposed in samples from a stranded adult that possessed no superficial epidermal layers (Fig. 9b), probably due to autolysis/decomposition.

Figure 9.

A: Scanning electron micrograph images showing the irregular nature of the superficial epidermis of a “rough-skinned” southern right whale calf. Note the exposed keratinocyte rosettes around and superficial to the dermal papillae (arrows, original magnification 100×). B: Exposed keratinocyte rosettes around and superficial to the dermal papillae (arrow) of the skin of a stranded adult southern right whale. Decomposed dermal papillae (d). Absence of stratum corneum, probably due to decomposition (original magnification, 100×).

Histological and ultrastructural features of the epidermis.

Because the ultrastructural features of the southern right whale calf epidermis have been reviewed in detail by Pfeiffer and Rowntree (1996), this description provides only a limited review as well as adding information on animals from other age groups.

Histologically, the epidermis in both adults and calves consisted entirely of stratified squamous epithelium making up three distinct layers, namely (from outermost to innermost), stratum corneum, stratum spinosum, and stratum basale (Fig. 10). Many of the biopsied and stranded samples seemed to have lost the stratum corneum or only small portions of this layer were present, which indicates its friable nature. However, all sections that possessed stratum corneum cells (from both rough and smooth-skinned calves and juvenile and subadult samples) revealed the presence of keratin in these superficial cells. Neither a stratum granulosum nor a stratum lucidum was observed (Fig. 11).

Figure 10.

Longitudinal section through the integument of a neonatal southern right whale. Epidermis (E), stratum corneum (sc), stratum spinosum (ss), stratum basale (sb), reticular dermis (rd), hypodermis (H) infiltrated with collagen fibers (pink lines) and adipocytes (white spaces), superficial fascia (Sf). Hematoxylin and eosin stain, whole-mount = 7.8 cm).

Figure 11.

A,B: Structure of the integument of rorquals (A) and toothed cetacea (B). Legend: 1 = epidermis; 2 = dermal papillae; 3 = dermis; 4 = hypodermis; 5 = subcutaneous musculature; 6 = bundles of collagen fibers; 7 = bundles of elastin fibers; 8 = adipocytes (from V. Sokolov, 1955).

The stratum corneum consisted of multiple layers of stratified, squamous keratinocytes, with their long axes parallel to the skin surface. Most cells possessed flattened, moribund nuclei, due to the keratin in their cytoplasm. The presence of nuclei indicated that the process of keratinization in these cells was not complete, and the nature of this layer could, therefore, be described as parakeratotic. Within pigmented epidermis, most of the stratum corneum cells possessed melanin granules (Fig. 12a), usually located at the base of the cells, surrounding the nuclei.

Figure 12.

A: Stratum corneum (sc) and stratum spinosum (ss) layers of the epidermis of an adult southern right whale. Note melanin granules stained black (arrow, hematoxylin and eosin [H&E] stain; original magnification, 200×). B: Dermal papilla (DP) protruding into the stratum spinosum of a juvenile southern right whale. Note flattened stratum spinosum cells along the sides and tip of the papilla (arrows), melanin granules (m) stained black, and stratum basale (sb) (H&E; original magnification, 200×).

The epidermal cells deep to the parakeratotic stratum corneum comprised a typically mammalian stratum spinosum. The stratum spinosum was the most extensive of all the epidermal layers. The spinosal cells were rounded, oval, or polyhedral in shape, becoming increasingly flattened near the stratum corneum (Fig. 12a). At all the body positions studied, tightly packed spinosal cells occurred along the sides and tips of the dermal papillae (Fig. 12b), possibly forming the rosettes mentioned above.

Melanin granules were present in the cytoplasm of most cells, near the nucleus (Fig. 13a). The nuclei in this layer were more complete in presentation and occurred in a larger number of cells when compared with the nuclei of the stratum corneum cells. When viewed using light microscopy, the cell boundaries in this region appeared very thick. Transmission electron microscopy revealed that these thick boundaries were formed by highly folded cell membranes and desmosomes (Fig. 13a,b). Tonofilaments, arranged in parallel bundles, were present in all cells in the stratum spinosum (Fig. 13c). Ultrastructurally the large spinosal cell nuclei were irregular in shape with generally centrally located nucleoli (Fig. 13a). Lipid droplets and large groups of glycogen granules were present in the cytoplasm of spinosal cells (Fig. 13d). Collagen and elastin fibers were more abundant in the cells of the stratum spinosum of flukes and flippers than in any other location.

Figure 13.

A: Transmission electron micrographs showing the presence of melanin granules (m, black dots) around the nuclei of stratum spinosal cells. Note the thick cell boundaries formed by inter-folding cell membranes (i), nucleolus (n; original magnification, 12,000×). B,C: The extensive interfolding of stratum spinosum cell membranes (i) connected by desmosomes (d). Tonofilaments (t) are present in parallel bundles within these cells; melanin granules (m) are also present (B original magnification, 4,500×; C original magnification, 5,000×). D: Large groups of glycogen granules (g) in the cytoplasm of spinosal cells (original magnification, 6,000×). E: The stratum basale of the epidermis consisted of a layer of variably shaped keratinocytes (k), which interdigitate with the basal lamina (arrows) separating the epidermis (Ep) and the dermis (De). Collagen fibers (c; original magnification, 7,500×).

The stratum basale of the epidermis consisted of a layer of variably shaped keratinocytes, which interdigitated with the basal lamina separating the dermis and epidermis (Fig. 13e). The basal cells had basally located oval nuclei and contained numerous mitochondria, tonofilaments associated with desmosomes, and lipid droplets. The surfaces of adjacent cells interdigitated extensively with numerous desmosomes present. These interdigitations produced wide areas of apparent intercellular space, that were caused by the interfolding of the undulating adjacent cell membranes, with greater numbers of desmosomes than found in either of the other strata (Fig. 13e). In pigmented areas, melanocytes were present among the basal cells (Fig. 13e) and occasionally in the first few layers of the stratum spinosum. These specialized cells were large and well developed with typical dendritic processes and melanosomes.

Melanosomes, and consequently melanin granules, were most abundant in the stratum basale. A basement membrane separated the dermis and the epidermis but numerous membranous undulations of the basal cells maintained contact with the basal lamina and these layers (Fig. 13e).

Histologically, the only detectable difference between the epidermal strata of gray morphs, partial-gray morphs, and dark-skinned animals was that the concentration of melanin granules was visibly reduced in the former two color variants. Smooth-skinned calves and adults (Fig. 12a) appeared to possess more melanin granules than rough-skinned calves.

Histological and ultrastructural features of the dermis and hypodermis.

The dermis was divided into a papillary and reticular layer (Fig. 14a). Highly elongated macroscopic dermal papillae interdigitated extensively and distinctly with epidermal rete and were abundant throughout the integument along the body. The basal margin of the papillary dermis was composed of scattered adipocytes that infiltrated irregular, white fibrous connective tissue strands. Extensive vascularization and innervation were evident, with nerves extending from the hypodermis to the base of the dermal papillae and some blood vessels and nerve fibers extending along the dermal papillae (Fig. 14b,c). The reticular dermis consisted of tightly packed collagen fibers lying parallel to the long axis of the whale's body (Figs. 10, 14c). These fibers formed a thick network with essentially no adipocytes present, effectively creating a narrow “fat-free” band/zone (Figs. 10, 14c). Collagen fibers from this zone extended into the dermal papillae. Few elastin fibers extended through this layer. Deep to this layer, the hypodermis was defined by the increased presence of adipocytes. Adipocyte cell size was not measured, but, together with the number of adipocytes, seemed to increase in a proximal direction, inversely proportional to the amount of connective tissue (Fig. 10). The collagen fibers began to form small bundles, arranged in various orientations, which were completely surrounded by large groups of adipose tissue (Fig. 14d,e). This layer formed the majority of the southern right whale integument. A thin layer of tissue (superficial fascia) connected the hypodermis to the underlying muscular layers (Fig. 10).

Figure 14.

A: Dermal papillae (p) reach from the base of the papillary dermis (PD) into the epidermis (E) and epidermal rete (r) interdigitate with the dermal papillae. The reticular dermis (RD) consists of dense collagen fibers (dark blue) with blood vessels (b) coursing through both layers (Ayoub-Shklar, Mag 25×). B: Blood vessels (b) extending from the papillary dermis into dermal papillae and between epidermal rete (hematoxylin and eosin [H&E] stain; original magnification, 100×). C: The reticular dermis consists of tightly packed collagen bundles (arrows) forming a “fat-free” zone. Blood vessels (b), shown in irregular cross-section, course through this layer (H&E; original magnification, 25×). D: A nerve (n) extending through a collagen fiber bundle (c), surrounded by adipocytes (a), within the hypodermis (H&E; original magnification, 100×). E: Vascularization (b) is evident within collagen bundles of the hypodermis. Note the various orientations of the collagen bundles. Only remnants of adipocytes are visible (arrow) due to autolysis (H&E; original magnification, 25×). F: Longitudinal section through the bonnet callosity (callosity on the anterior tip of the upper jaw) of a stranded neonate revealing a hair follicle (f), deep to the epidermis (H&E; original magnification, 8×). G: Photomicrograph of the base of the hair follicle (f) in F, showing the blood sinus (b) appendage between the inner (i) and outer dermal (o) connective tissue sheaths (H&E; original magnification, 25×).

Staining revealed that the white connective tissue in both the papillary and reticular dermis (and including the flippers and flukes) consisted almost entirely of collagen fibers infused with small amounts of elastin fibers.

Histological structure of hair follicles and callosity “stalks.”.

Except for a slightly thicker stratum corneum, the integumentary layers forming callosities were not found to be structurally different from the integumentary structure found along the remainder of the body of southern right whales. The hairs associated with the callosities and present on the snout and chin projected approximately 1–2 cm above the epidermis and arose from specialized follicles that extended approximately 1.1 cm into the blubber, deep to the epidermis and papillary dermis (Fig. 14f). The follicle was an innervated, double-walled structure that contained blood sinuses between inner and outer dermal connective tissue sheaths (Fig. 14g).

The pigmented epidermal projections (“stalks”) that occurred within callosity formations (Fig. 2a) were examined in a stranded juvenile and consisted of nucleated and viable stratum spinosal cells that were not extensively flattened (Fig. 15). No true stratum corneum was discernible.

Figure 15.

A longitudinal section through an epidermal “stalk,” from the head of a stranded juvenile shows this structure consisting of viable, nucleated stratum spinosal cells (n) (hematoxylin and eosin stain; original magnification, 200×).

Blubber Thickness

Neonates are the only age class for which sufficient data exist to examine trends in blubber thickness over the body in any detail (Table 1). Blubber thickness varied along the dorsal, lateral, and ventral planes and in different positions along these planes (1.5–10.3 cm). Dorsal blubber (n = 4) showed little change in thickness from directly behind the head (position 1) to the region parallel to the axilla (position 2), but then gradually thickened with the region at the anterior margin of the peduncle (position 5) being approximately twice as thick as position 2. Lateral blubber (n = 3) was highly variable in thickness at position 1 (possibly because of the proximity to the flipper insertion) and seemed to decline from position 3 (midway between positions 1 and 5) to position 5 (although one individual had atypically thick blubber at this position). Ventral blubber (n = 2) exhibits a similar trend to that of dorsal blubber, decreasing in thickness from position 1 to position 2, but then steadily increasing in thickness, although position 5 was only approximately 50% thicker then position 2.

Biopsies were taken in the vicinities of positions 3 or 4 (midway between positions 3 and 5) on the dorsolateral plane. The deepest blubber sample (excluding pigmented epidermis) retrieved from an early season calf measured 9.7 cm (n = 20), 12.7 cm from a late season calf (n = 18), 17.2 cm retrieved from an early season adult (n = 13), and 21.2 cm from a late season adult (n = 9) (Table 4). None of the biopsies retrieved showed histological evidence of the superficial fascia (the innermost boundary of the integument), which indicates that full core samples were not obtained. Statistical analyses were, therefore, not applied to the above data as these results are more likely to reflect sampling differences, that is, length of biopsy head (Reeb and Best, 2006), than biological changes. Nevertheless, it is clear from a comparison of full-core blubber thicknesses in stranded neonates with the incomplete cores obtained from free-swimming calves and adults, that considerable fattening must occur after birth and between first-year and adulthood.

Table 4. Depths (in cm) of biopsied blubber samples retrieved from southern right whale cowsa and calves (epidermis excluded)
Early season calves (n = 20)Early season cows (n = 13)Late season calves (n = 18)Late season cows (n = 9)
  • a

    Based on the assumption that all adults accompanying calves were their lactating mothers.

4.25.51.519.5
7.41.81.85.0
1.55.02.321.2
7.26.53.420.5
8.317.21.817.3
2.55.52.420.7
3.16.43.920.1
4.86.23.413.0
9.712.66.612.0
8.87.37.7 
1.42.812.7 
7.16.73.4 
8.96.99.7 
6.4 5.6 
8.3 4.3 
1.8 7.4 
3.3 8.4 
3.7 8.0 
6.6   
3.9   
Average = 5.4Average = 7.0Average = 5.2Average = 16.6

DISCUSSION

General Characteristics of Southern Right Whale Skin

Although, researchers and Eskimo captains claimed that early season calves of bowhead whales had especially thick epidermis (Eschricht and Reinhardt, 1866; Haldiman et al., 1982, 1985; Haldiman and Tarpley, 1993), the differences in epidermal thicknesses between seasonal and age groups of southern right whales were not significant. It is possible, however, that observers of the bowhead whale may have been referring to the epidermis of pre-ecdysal (pre-moult) neonates, which may be slightly thicker than in other calves (Reeb et al., 2005b). No trends in the variation of epidermal thickness along the bodies of stranded animals were obvious, although individual variation was noted along all positions.

This study supports the observations made by Ridewood (1901), when he described the bonnet (large callosity located on the tip of the snout) of the southern right whale as a “circumscribed tract of skin, where, for some reason not yet apparent, the cornified layers fail to rub off at their normal rate, but remain and accumulate to produce a hard mass, projecting above the general surface of the epidermis as a kind of corn.”

Callosities of southern right whales vary from mostly smooth in fetuses with a molded or wrinkled appearance (Lönnberg, 1906; Matthews, 1938) to very rough in adults with tall, irregular epidermal projections and deep clefts. This observation confirms other observations that only some time after birth, do they become roughened and pitted and almost completely covered with colonies of species of amphipod crustaceans of the family Cyamidae (whale-lice) (Roussel de Vauzème, 1835; Payne et al., 1983; Rowntree, 1983). The postnatal ecdysal moult may represent a critical initiation of this process (Reeb et al., 2005b).

Lamarck (1802, in Darwin, 1854) first described the barnacles found on the callosities of southern right whales as Tubicinella sp. Pilsbry (1916) stated that almost all the recorded incidences of Tubicinella were from Southern Hemisphere right whales and that only one record of this barnacle had been made in the Northern Hemisphere (in 1650). It is, therefore, curious that these barnacles have not been recorded on Argentinian and Australian right whales. This finding is possibly due to the lack of boat-based field-work with these populations and/or the difficulties involved with attending strandings in these areas, or may simply be an oversight.

The stiff hairs and hair follicles found on the heads of southern right whales are comparable to those described in the sei whale by Nakai and Shida (1948). The innervated nature and presence of “blood sinuses” possibly re-affirm Slijper's (1962) opinion that these structures are not hairs at all, but tactile organs analogous to vibrissae found in terrestrial animals. Distinct nerve nets and blood sinus appendages have been associated with these hairs in bowhead whales (Haldiman et al., 1981, 1985; Haldiman and Tarpley, 1993) and may indicate a tactile function. The number, spacing, and distribution of these hairs on the snout and chin of southern right whales would seem to support such a function, possibly allowing rapid detection of changes in prey density and, thus, enabling the whale to stay within the densest part of the swarm (North Atlantic right whales, Mayo and Marx, 1990).

Microscopic Characteristics of Southern Right Whale Skin

Superficial epidermal features.

The absence of diatomaceous concentrations, and the presence of various microbes, on the surface of the skin of southern right whales examined in this study is discussed in more detail elsewhere (Reeb et al., manuscript in preparation). The observations of epidermal sloughing in animals sampled in South African coastal waters during winter months, coupled with histological evidence from Antarctic waters during mid-summer, suggest that sloughing continues year-round. Determining possible differences in cellular proliferation rates, using PCNA techniques, is recommended for future studies.

The honeycomb pattern formed by flaking, superficial epidermal cells, and smooth patches of undisturbed skin were seen on the skin surface of smooth-skinned calves. The presence of both skin patterns (i.e., honeycomb and smooth) possibly represents different stages of the epidermal sloughing cycle, with the smooth patches not having been shed yet. The “unpitted” nature of the smooth patches further suggests that such calves may be undergoing their first “adult-like” epidermal exfoliation, after postnatal ecdysis (Reeb et al., 2005b).

Histological and ultrastructural features.

A recognizable division of the epidermis into a stratum basale, stratum spinosum, and a parakeratotic stratum corneum is supported in this species, although only a stratum basale and externum have been previously recognized by other researchers (Pfeiffer and Rowntree, 1996). The accumulation of melanin granules (in pigmented areas) and basophilic nuclear remnants (including pyknotic nuclei, i.e., nuclei in a degenerative state) present in the stratum corneum give this layer a true (nonpathological) parakeratotic nature. This condition has been described in other cetacean species (Simpson and Gardner, 1972; Spearman, 1972; Ling, 1974; Menon et al., 1986; Elias et al., 1987; Haldiman et al., 1985; Haldiman and Tarpley, 1993).

The polyhedral cells of the stratum spinosum and cells of the stratum basale contained mitochondria and melanin. Keratohyalin granules were present in spinosal cell cytoplasm and abundant tonofilaments were associated with desmosomes. Lipid droplets were also detected as cellular components, essentially conforming to the epidermal studies described for other cetacean species (Ling, 1974; Haldiman et al., 1985; Menon et al., 1986; Elias et al. 1987; Haldiman and Tarpley, 1993).

Rosettes formed by keratinocytes above epidermal rods were not reported on the surface of the skin in southern right whale calves by Pfeiffer and Rowntree (1996). In this study, however, using SEM, the rosettes were detected in all age groups, and for all the samples from various positions on the body on the surface of the skin (except in some taken from rough-skinned calves). These structures have been described on the surface of adult bowhead whale skin (Haldiman et al., 1985), also seen superficially using light microscopy as “dots” (Reeb et al., 2005b).

The high prevalence of cytoplasmic lipid droplets in lipokeratinocytes is a common feature of both the southern right whale and all other cetacean species reported thus far (Stromberg, 1985; Menon et al., 1986; Elias et al., 1987; Pfeiffer and Jones, 1993; Pfeiffer and Rowntree, 1996). The integumentary epidermal cells of the cetacean stratum corneum and stratum spinosum are, thus, properly termed lipokeratinocytes (Elias et al., 1987). An important and unique finding in the right whale lipokeratinocyte is the frequent intimate association of lipid droplets with the nucleus that is thought to facilitate the energetics of nuclear metabolism (Pfeiffer and Rowntree, 1996). Lipokeratinocyte lipid storage droplets in other cetacean species studied (Pfeiffer and Jones, 1993) have also been thought to support cellular metabolism rather than functions related to insulation or secretion.

The bowhead whale has the thickest epidermis of any cetacean studied (up to 25 mm) (Tomilin, 1957; Albert et al., 1980; Durham, 1980; Haldiman et al., 1981, 1985; Haldiman and Tarpley, 1993). Concentrations of epidermal rods arising from the stratum basale cells around the tips of the dermal papillae are characteristic of thick, hypertrophied, and acanthotic epidermal regions of the parakeratotic stratum corneum of the bowhead whale (Haldiman et al., 1981, 1985; Haldiman and Tarpley, 1993). This integumentary specialization is thought to function in holding together the thick epidermis. Besides perhaps providing insulation in cold, Arctic waters, the thickness of the bowhead epidermis as well as the presence of epidermal rods, possibly act as barriers against mechanical injury. Bowhead whales routinely break new ice at least 18 cm thick, and Inuit hunters have reported that bowheads may break ice up to 60 cm thick to breathe (George et al., 1989). Although the southern right whale is not as pagophilic as the bowhead whale, its epidermis is second only to the bowhead's in thickness. The presence of epidermal rods, the extensive interdigitation seen between stratum spinosum and stratum basale cells, the high concentrations of desmosomes and the striking association between the rete pegs and dermal papillae may all contribute to the mechanical stability required for this species to possess a thick epidermis. Perhaps such mechanical stability is an advantage for a species that seasonally inhabits the extreme near-shore region, constantly coming into close proximity with the sea floor and/or sea floor structures (e.g., rocks, reefs). Alternatively, it may be an adaptation to the high levels of bodily contact (including the use of callosities) exhibited by right whales in socially active groups. The far-reaching dermal papillae may also make it possible for nutrients to reach the uppermost layers of the epidermis.

The extensive interdigitation of the dermis and epidermis is a striking feature of the integument of this species and other cetaceans. It has been suggested (Ling, 1984) that, because cetaceans do not have a pelage, the ability of the epidermis to take over the role of friction reduction is aided by the greatly folded nature of the junction between the epidermis and the dermis. This feature may have a protective function against the hydrodynamic friction of swimming (Giacometti, 1967). Papillae are also penetrated by blood vessels, bringing vascularization very close to the skin surface (Slijper, 1962; Yablokov et al., 1974) and, thus, possibly maintaining tissue temperatures at an optimum level for the rapid rate of mitosis (Ling, 1974) evident in the epidermis of some cetaceans (Palmer and Weddell, 1964; Brown et al., 1983; Hicks et al., 1985; St. Aubin et al., 1990). Elaboration of dermal papillae may also increase body surface area, with consequences for thermoregulation.

A distinctive “fat-free” zone consisting of collagen fibers makes up the reticular dermal layer, which corresponds to previous findings for other members of the Balaenidae (Sokolov, 1960, 1962b, 1982). Sokolov (1960) found that the North Pacific right whale (E. japonica) possessed well-developed, elastic fiber networks within the dermal and hypodermal integumentary layers, whereas only a few elastic fibers were detected in E. australis using Weigert's-Resorcin stain. Both of the last-mentioned traits are more similar to odontocete integumentary structure than to balaenopterids (Yablokov et al., 1974).

In the bowhead whale, Haldiman and Tarpley (1993) describe the innermost (deepest) aspect of the blubber layer as being bounded by a 1–2 mm thick layer of two highly tendinous connective tissue sheets. The fibers that make up these sheets are arranged perpendicular to each other (Haldiman et al., 1982). These authors state that a true hypodermis extends between the innermost tendinous layer and the underlying muscles and other organs. This thin connective tissue layer was not found in the histological sections used in this study. Similarly, histological inspection did not reveal the presence of any discernible collagenous layer interrupting the hypodermis, as has been described in Nova Scotian sei whales (Ackman et al., 1975). In this study, southern right whales possessed uninterrupted collagen bundles surrounded by large amounts of adipose tissue that occurred below the dermis. This collagen bundle and adipocyte arrangement is considered, here, to compose the hypodermis. It is, however, acknowledged that the varying amounts of adipose tissue contained within the hypodermis depend upon the animal's age and nutritional status (Haldiman and Tarpley, 1993). It may, therefore, be possible that this innermost layer only becomes evident during the fattening/feeding stages of the animal's nutritional cycle, being comparable to the “isterlag” or “leaf fat” described by Heyerdahl (1932), Tveraaen (1935), and Pedersen (1950) in very fat Antarctic baleen whales. Ackman et al. (1975) have likened the layer of collagenous and elastic fibers, which interrupts the hypodermal layer of the integument of Nova Scotian sei whales (also caught during the summer feeding season), to this layer.

Blubber thickness.

The thick blubber layer found in right whales (Slijper, 1962; Omura, 1969; Angell, 2005) is second only to that found in bowhead whales (Haldiman and Tarpley, 1993). However, unlike the bowhead whales, right whales do not spend their lives in polar waters. Right whales also are not the only migratory mysticetes enduring months of low food intake in lower latitudes during calving. The question, therefore, arises why these members of the Balaenidae should possess such a thick integument. It is here suggested that this feature is linked to the evolutionary origins of mysticetes. Fordyce (1980) states that the earliest known mysticetes and odontocetes are New Zealand Early Oligocene forms. Assembled evidence indicates that the evolution of mysticetes was probably induced by plankton productivity changes (and consequent increases in zooplankton availability) associated with the initiation of the psychrosphere during the Early Oligocene and the Circum-Antarctic Current (CAC) in Mid-Oligocene times (Fordyce, 1977). Glaciation in Antarctica during the Late Eocene affected temperature regimes, nutrient availability and hence productivity in Antarctic and Subantarctic waters (Kennett et al., 1975; Hayes and Frakes, 1975). The establishment of the CAC meant that, from mid-Oligocene times onward, areas such as the Campbell Plateau (which border the Sub-Antarctic region) were affected by these climatic changes. Shackleton and Kennett (1975) stated that temperatures on the Campbell Plateau dropped from 19°C in the Early Eocene to 11°C in the Late Eocene and to 7°C in the Oligocene. The Balaenidae are thought to be the oldest of the modern mysticete families, evident in the fossil record during the Mid-Oligocene (Fordyce, 1980). This time period corresponds with the period that the cold, Antarctic-derived current (i.e., CAC) began to flow. Presumably bulky, slow-moving, filter-feeding mammals would need to develop a thick insulatory integument while living in such a cold-water environment.

Alternatively, the evolution of balaenid feeding strategy, which depends on finding ultra high concentrations of prey rather than using behavioral techniques to concentrate it (as in most other mysticetes), may have made them more susceptible to periodic prey shortages, leading to the need for increased fat storage.

The blubber thickness results obtained from a small number of stranded neonates cannot be used to make any general inferences about this character in free-swimming right whales. However, it is interesting to note that, along the dorsal plane, the blubber thickness was similar at position 1 and position 2. This area between positions 1 and 2 corresponds to the “fat roll” seen by the authors on adult southern and northern right whales, which has been interpreted as a temporary structure associated with nutritional status. In the neonates sampled (Table 2), there is a general trend for the mid-dorsal blubber to increase in thickness in a craniocaudal pattern. This pattern has been described previously in other mysticetes (Lockyer et al., 1985). The lateral samples include measurements taken from a juvenile and the marked decrease in blubber thickness in a craniocaudal direction, especially in Position 5, helps create the laterally compressed, stream-lined tailstock. Unfortunately, the lateral location of these samples makes them incomparable to results from other investigations (Ackman et al., 1975; Lockyer et al., 1985), but the laterally compressed nature of the cetacean peduncle (and the underlying structure of the blubber) has been proposed as a mechanism for creating elastic energy that assists in propulsion (Summers, 2001; Hamilton et al., 2004).

The deep-core sampling technique was a successful first attempt at obtaining representative integument samples from a free-swimming balaenid. Histological analysis, as well as ultrasound blubber thickness measurements (Angell, 2005), indicate that complete cores were not retrieved from animals, adults in particular. However, on a structural level, samples from stranded animals have been used to supplement the biopsies. The large difference between blubber thickness of early and late season cows should only be used as a gauge of the increased operator efficiency of the biopsy system, and not interpreted as seasonal variation in blubber thickness.

This study presents the first comprehensive description of the southern right whale integument, using both stranded material and samples collected from free-swimming whales in South African as well as Antarctic waters. Future studies should include further attempts to collect representative (i.e., full-core) integumentary samples, as well as techniques to determine whether cellular proliferation rates of epidermal cells differ between whales in summer feeding and winter breeding grounds.

Acknowledgements

The authors thank Yolanda Davies, Helen Ilsley, Dr. Maureen Duffield, Mary Wolfe, Sharon Marshall, Heather McLeod, Dr. Dirk Lang, and Liz Van Der Merwe from the Departments of Human Biology and Anatomical Pathology, Faculty of Health Sciences, University of Cape Town, for advice and technical assistance. Linda Bisset from the S.A. Museum for SEM assistance. Rudy Cloete-Hughes, Derek Kemp, and Mark Addison are thanked for skippering during field work. We are grateful to Steve Stafford and Susan and Basie Uys for providing accommodation in Gansbaai and Witsand. The authors express their gratitude to Dr. Carolyn Miller-Angell for constructive comments on the manuscript and to the editors for inviting us to submit this manuscript for publication in the special issue. We acknowledge the funding provided by the National Research Foundation to D.R.

Ancillary