Acute sun damage and photoprotective responses in whales

Abstract

Rising levels of ultraviolet radiation (UVR) secondary to ozone depletion are an issue of concern for public health. Skin cancers and intraepidermal dysplasia are increasingly observed in individuals that undergo chronic or excessive sun exposure. Such alterations of skin integrity and function are well established for humans and laboratory animals, but remain unexplored for mammalian wildlife. However, effects are unlikely to be negligible, particularly for species such as whales, whose anatomical or life-history traits force them to experience continuous sun exposure. We conducted photographic and histological surveys of three seasonally sympatric whale species to investigate sunburn and photoprotection. We find that lesions commonly associated with acute severe sun damage in humans are widespread and that individuals with fewer melanocytes have more lesions and less apoptotic cells. This suggests that the pathways used to limit and resolve UVR-induced damage in humans are shared by whales and that darker pigmentation is advantageous to them. Furthermore, lesions increased significantly in time, as would be expected under increasing UV irradiance. Apoptosis and melanocyte proliferation mirror this trend, suggesting that whales are capable of quick photoprotective responses. We conclude that the thinning ozone layer may pose a risk to the health of whales and other vulnerable wildlife.

Figure 1.

(a) Differences in skin colour (SC) and time spent at the surface (ST) among blue (Bm), sperm (Pm) and fin whales (Bp). (b) Melanocyte counts in blue (Bm, n = 63), sperm (Pm, n = 17) and fin whales (Bp, n = 46).

Figure 2.

Typical images of skin lesions. (a) Gross blistering on the dorsal surface of a blue whale, (b) bite marks on the dorsal surface of a blue whale seen as oval-shaped lesions with a sunken perimeter, (c) bite marks seen as parallel rakings, (d) cytoplasmic vacuolation (400×), (e) intracellular oedema (250×) and (f) microvesicles (50×). Lesions are indicated by arrows.

Figure 3.

Prevalence of gross blisters and microscopic epidermal abnormalities in blue whales (pale grey bars), sperm whales (dark grey bars) and fin whales (black bars). Sample sizes are indicated in the figure. Bars = ±s.e.m.

Figure 4.

Presence of apoptotic cells (AC) in skin sections. (a) TUNEL-stained fin whale skin showing AC (round-stained nucleus indicated by arrows) throughout the epidermis (category 3 AC; bar = 100 µm). (b) TUNEL-stained sperm whale skin with category 2 AC (bar = 100 µm). Melanin pigments are seen as black granular material. (c) Prevalence and categories of AC in blue whales (pale grey bars, n = 18), sperm whales (dark grey bars, n = 11) and fin whales (black bars, n = 14). Bars = ±s.e.m.

Figure 5.

Temporal changes in the prevalence of blue whale skin lesions (blisters, black line; bite marks, pale grey line; cytoplasmic vacuolation, dark grey line). Sample sizes are indicated in the figure. Bars = ±s.e.m.