Abstract
We report on an occurrence of ocular albinism in sub-Antarctic fur seal (Arctocephalus tropicalis) pups born on Marion Island, Prince Edward Archipelago. While previous observations have documented pups with atypical lanugo pelage colorations, this is the first case involving hypopigmentation of both fur and other tissues, including the eyes and nails. During the austral summer of 2021/22, we encountered four sub-Antarctic fur seal pups displaying this anomalous pigmentation. These anomalous individuals were found along two beaches on the island’s western side and one beach on the eastern side during an island-wide fur seal census. Although the characteristics observed strongly suggest ocular albinism, confirmation would be necessary through genetic analyses. The absence of melanin in mammalian eyes is known to compromise visual acuity, which may likely result in reduced survival beyond the weaning period, explaining the paucity of such adults in this well-observed population.
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Introduction
In mammals, pigmentation of the skin, hair, and eyes is controlled by the amount of melanin produced by melanocytes (Acevedo et al. 2009a; Utzeri et al. 2021). Two types of melanin are responsible for this pigmentation, namely eumelanin which controls black-to-brown pigmentation, and pheomelanin which results in yellow-to-red pigmentation (Utzeri et al. 2021). Anomalous pigmentation in mammals can be classified as albinism, leucism, melanism, and piebald, each of which differs in the resulting coat color (Acevedo and Aguayo 2008). As these anomalous traits are a result of genetic mutations and can be inherited, it is important to study and document them as they can give vital insight into how populations are shaped by migration. For example, Hoffman et al. (2018) illustrated the nature of migration through the provenance and prevalence of cream coloration in Antarctic fur seal (Arctocephalus gazella) populations that recovered and spread to different localities after the cessation of commercial harvesting. They showed that the South Georgia population, believed to be responsible for most of the global recovery of the species, was the source of anomalous cream-colored fur seals seen in several other localities.
Albinism is a congenital genetic condition characterized by the reduced or complete absence of melanin in the eyes, skin, hair, and nails (Acevedo et al. 2009a). The hypopigmentation of the eyes differentiates albinism from other types of anomalous pigmentations in mammals which only affect the skin and hair (Fertl and Rosel 2009). Albinism can affect the eyes with little or no hypopigmentation of the skin and hair (King and Summers 1988). This is known as ocular albinism and it is characterized by hypopigmentation and translucency of the iris, reduced visual acuity, and reduced pigmentation of the retinal pigment epithelium (Grønskov et al. 2007). As a result, individuals with ocular albinism have reduced visual acuity with blue or brown irises (see Grønskov et al. 2007).
In Southern Ocean pinnipeds, anomalous pigmentation is well documented in Antarctic fur seals for which several kinds of hypopigmentation have been reported, including individuals with light brown, pied, tiger-like, and tricolor pelages (Acevedo et al. 2009a), as well as leucism which has been documented in low proportions at several breeding locations (Bonner 1968; Hofmeyr et al. 2005; De Bruyn et al. 2007; Acevedo et al. 2009a; Wege et al. 2015; Peters et al. 2016; Romero and Tirira 2017). In contrast, there are fewer reports of anomalous pelage colorations in the closely related sub-Antarctic fur seal (A. tropicalis). Leucism has been documented in a single adult male sub-Antarctic fur seal on Gough Island (Jones et al. 2019), while pups of this species have been documented with anomalous colorations of their lanugo fur on Marion Island, but all had normal pelage coloration once they had moulted into their sub-adult coats (du Toit et al. 2019). Here we report on four sub-Antarctic fur seal pups born at Marion Island with hypopigmentation of the eyes as well as their lanugo fur and nails, a combination which has not previously been recorded on the island and which may be the first case of ocular albinism in sub-Antarctic fur seals. This type of hypopigmentation is rare, and has only recently been documented in northern fur seals Callorhinus ursinus (NOAA 2022). Other reports of albinism in seals were documented on Weddell seals Leptonychotes weddelli at Cape Shirreff, Livingston Island (Acevedo et al. 2009b).
Materials and methods
Marion Island is one of two sub-Antarctic islands in the southern Indian Ocean that form the Prince Edward Islands (46.897°S 37.726°E, Fig. 1). The islands host the largest sympatric breeding population of sub-Antarctic and Antarctic fur seals (Wege et al. 2016) which have been intensively studied since the 1970s (Bester et al. 2011; Oosthuizen et al. 2016; Wege et al. 2016). The long-term monitoring studies of these species have afforded researchers with an opportunity to consistently document and photograph unusual behavior or characteristics they come across (De Bruyn et al. 2007, 2008; du Toit et al. 2019). Fur seal pups are routinely counted at several monitoring beaches on Marion Island for population monitoring purposes and demographic studies, and a full island count of both fur seal species is done every 5 and 10 years on Antarctic and Sub-Antarctic fur seals, respectively (Hofmeyr et al. 2006; Wege et al. 2016). During this count, a researcher visits every accessible beach on the island, counting all live and dead pups of each species. Counts are undertaken during January and February, when the pups are still small and aggregated on beaches (Wege et al. 2016). In addition, the consistent presence of field researchers for more than 40 years associated with the southern elephant seal Mirounga leonina mark recapture study (Oosthuizen et al. 2010, 2011, 2019, 2021; Pistorius et al. 2011), has provided observational opportunity for anything unusual.
Results and discussion
During the most recent total island count (2021/2022 breeding season), four sub-Antarctic fur seal pups with anomalous pelages were observed. They were seen between 22 Jan and 12 Feb 2022, with three observed on the western side of the island at Triegaardt Bay and Swartkop Cove, and one on the eastern side at Landfall Beach (Fig. 1, Table 1). The pups had reddish-gold lanugo fur (in contrast to the usual black, Fig. 2A, B, C) and had blueish-white eyes that were watery and covered in rheum (Fig. 2C). All observed pups had signs of reduced visual acuity as they were unresponsive to movement in front of them. While their flippers appeared normal, their nails exhibited a lighter shade compared to the typical dark black nails of sub-Antarctic fur seal pups (see Fig. 2D, E). The pup found at Swartkop Cove displayed white vibrissae and eyebrows, whereas the other pups exhibited a combination of white and black vibrissae. Despite their visual impairment, all four pups appeared to be in a healthy condition and were physically restrained for the collection of biopsy samples and determination of their sex (refer to Table 1). On a subsequent visit to Landfall Beach on March 1, 2022, a pup with anomalous pelage was observed to suckle from its mother, who displayed normal pelage coloration. The presence of the researcher caused the adult female to hastily retreat into the ocean, precluding the capture of photographs. The pups located at Triegaardt Bay and Swartkop Cove were resighted again on May 2 and May 4, 2022, respectively. By this time, the pups had undergone a moulting process, shedding off their reddish-gold lanugo coat and adopting a dark grayish appearance which is more consistent with the typical coloration of the species. However, their moulted coats were still distinguishable from those with normal coloration and their eyes remained light in color, with a milky appearance, and were still covered in rheum (see Fig. 3).
A Albino sub-Antarctic fur seal pup from Swartkop Cove on the left, next to a normal pup with a black, glossy, lanugo coat. The bottom of the atypical pup’s eyes is covered with rheum. B The pup with atypical coloration at Landfall Beach, next to a pup with typical coloration. The eyes of the atypical pup are surrounded by rheum. C Comparison of the eyes of the albino pup and normal pup. The normal pup is indicated with an arrow. D Atypically colored nails of the albino pup from Landfall Beach. E Sub-Antarctic fur seal pup after moulting the typical lanugo black fur coat with typical nails shown by the circle. Photograph credits: A: F van der Vyver, B, C and D: Y. Shihlomule
The observed anomalous coloration of the fur, nails, and eyes reported here suggests that this is the first documented case of ocular albinism in sub-Antarctic fur seals, distinct from other types of hypopigmentation that primarily affect the skin and/or fur. Albinism is attributed to genetic mutations in the tyrosinase gene that facilitates the biosynthesis of melanocytes which are responsible for melanin production (Grønskov et al. 2007). Albinism does not always result in complete white pigmentation of the skin or fur (Grouw 2013), and has only recently been documented in another fur seal species, where a Northern fur seal Callorhinus ursinus pup with reddish-gold fur, bluish-white eyes, and pale flippers was observed on Tyuleny Island, Sea of Okhotsk, Russia (NOAA 2022). Further genetic investigations are required to identify the specific mutations associated with ocular albinism in sub-Antarctic fur seals and elucidate how different mutations contribute to various degrees and different types of albinism. Notably, the sub-Antarctic fur seal pups on Marion Island displayed normal pigmentation in their flippers, unlike the light flippers observed in the C. ursinus pup (NOAA 2022). The sub-Antarctic fur seal shows a division of three evolutionary genetic lineages which are complex to distinguish geographically (Wynen et al. 2000). Therefore, documenting such sightings of this rare form of hypopigmentation is useful, as it may provide insight into gene flow and migration between populations in the Southern Ocean. Although the pups appeared physically normal, their impaired visual acuity may potentially impact their survival into adulthood.
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Acknowledgements
The Department of Forestry, Fisheries and the Environment provided logistic support within the South African National Antarctic Programme. The Department of Science and Technology, through the National Research Foundation, provided financial support.
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YS, FV and RJ were in the field, saw the Triegaardt Bay and Swartkop Cove sub-Antarctic fur seal with albinism, and took photos. YS saw the Landfall Beach sub-Antarctic fur seal pup with albinism, and took photos. DC was conducting seal research and EW was conducting sea-bird research in the area. The first draft of the manuscript was written by YS and all authors commented on the previous versions of the manuscript. EW made the map with locations where the albino pups were seen. All authors read and approved the final manuscript.
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All Marion Island Marine Mammal work has ethics clearance from the Animal Ethics Committee of the Faculty of Veterinary Science, University of Pretoria, under NAS003/2021 and is carried out under the permit granted by the Director-General: Department of Forestry, Fisheries and the Environment, South Africa.
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Shihlomule, Y.D., Weideman, E.A., van der Vyver, J.S.F. et al. First record of ocular albinism in sub-Antarctic fur seal (Arctocephalus tropicalis) pups on Marion Island. Polar Biol 47, 173–177 (2024). https://doi.org/10.1007/s00300-023-03217-6
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DOI: https://doi.org/10.1007/s00300-023-03217-6