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Skin condition of fin whales at Antarctic feeding grounds reveals little evidence for anthropogenic impacts and high prevalence of cookiecutter shark bite lesions

2022; Wiley; Volume: 39; Issue: 1 Linguagem: Inglês

10.1111/mms.12966

1748-7692

Helena Herr, Sacha Viquerat, Tobias Naujocks, Bertie Gregory, Abigail Lees, Fredi Devas,

Turtle Biology and Conservation

The skin condition of cetaceans, including scars, scratches, and injuries, can tell us a lot about the exposure to natural and anthropogenic impacts on individuals or populations (Baker, 1992; Herr et al., 2020; Kiszka et al., 2008; Van Bressem et al., 2006). Some features naturally accumulate over a lifetime and may be indicative of the age or sex of the animal (MacLeod, 1998). For example, many odontocete cetacean species accumulate scars inflicted by intraspecific interaction over their lifetime, with old individuals being most heavily scarred, or scarring only occurring in males as a consequence of male competition (Lee et al., 2019; Martin & Da Silva, 2006). Other features occur seasonally, like a yellowish skin coloration caused by diatoms accumulating on the skin of cetaceans during their stay in polar waters and being shed afterwards, during the dermal molt when the animals migrate to warmer waters (Bennett, 1920; Durban & Pitman, 2012; Hart, 1935; Mackintosh & Wheeler, 1929; Pitman et al., 2020). Presence of parasites may point to specific origins of migration (Iwasa-Arai et al., 2018). Cookiecutter shark (Istius spp.) bite lesions on cetaceans in high latitudes suggest movement outside the cold-water regions, as the known distribution of cookiecutter sharks is in warm temperate to tropical waters (Dwyer & Visser, 2011; Jones, 1971). Specific marks can be related to predatory scarring (Moore et al., 2003; Naessig & Lanyon, 2004) and certain characteristics tell of individual fates, such as injuries from ship strikes or interaction with fisheries (Bradford et al., 2009; Herr et al., 2020; Pettis et al., 2004; van Waerebeek et al., 2007). Reoccurring features among individuals of a population may inform about threats within their habitat (Bonneville et al., 2021; Kiszka et al., 2008; Panigada et al., 2006), and prevalent skin diseases can indicate poor habitat quality and environmental stressors (Van Bressem et al., 2009). Specific features may even serve as population markers (Best, 1977; Moore et al., 2003). After their near-extirpation by 20th century industrial whaling, fin whales (Balaenoptera physalus) of the Southern Hemisphere finally seem to be recovering (Herr et al., 2022). High densities and reoccurring large feeding aggregations at ancestral feeding grounds around the northern Antarctic Peninsula suggest increasing population numbers (Herr et al., 2022). However, the migratory origin of these animals feeding at the Antarctic Peninsula is not yet known. The population structure of Southern Hemisphere fin whales, which form a separate subspecies (Balaenoptera physalus quoyi) is yet unclear (Archer et al., 2019). It is unknown where the animals feeding at the Antarctic Peninsula migrate from, where they spend the remainder of the year, and where their breeding grounds are located. We collected high-resolution video imagery of fin whales at an Antarctic feeding ground during a dedicated abundance survey, using helicopter and drone supported cameras, and used the imagery for an assessment of the skin condition. We analyzed individual fin whales, looking for conspicuous features, including injuries, abnormal coloration, scars, and parasites as indicators for exposure to natural and anthropogenic impacts. We hypothesized that typical signs for environmental and anthropogenic impacts would be evident in the animals if they had been exposed to these effects during some part of their life history. Such information would be critical with regard to management and conservation of this recovering population, to identify and to mitigate identified pressures. Furthermore, it could provide insights on migratory origins and habitat during the breeding season. Video imagery of whales was collected during research expedition PS112 (March 18–May 5, 2018; Meyer & Wessels, 2018) of the German research ice breaker Polarstern to the Antarctic Peninsula. During an aerial survey using the on-board helicopter (BO-105), a RED Helium 6 K camera with Canon CN20 (50–1,000 mm) lens inside a GSS gyro-stabilized system attached to the helicopter was used to record fin whales encountered during survey effort from an altitude of 600 ft (~183 m). Survey effort was suspended for filming to provide sufficient time for documenting the animals. The animals were recorded from breaking the surface to submerging again, typically presenting the full length of their head and dorsum to the dorsal fin. Line-transect survey design prevented duplicate encounters of individual animals during survey flights. In addition to footage collected during the aerial survey, we launched drones (DJI Phantom 4 and Inspire II equipped with a Zenmuse X5S camera) during ship transit upon encounter of fin whales. Drones filmed the whales from an altitude of 100–150 m and did not approach the whales closer than 100 m to avoid disturbance. Altogether, 325 film sequences with a total runtime of 2.52 hr were recorded. For analysis, sequences containing complete surface intervals, showing fin whales from head to dorsal fin, were extracted and surfacing scenes clipped from these. The resulting data set consisted of 157 scenes of surfacings, adding up to a total runtime of 27 min. Scenes were screened by the same person for conspicuous features, using a video playback software (VLC player; https://www.videolan.org/vlc/). Conspicuous features were first described phenotypically. Based on the descriptions rather than presumed etiology, the following categories were established: circular white spot, pale patch, scar, dent, skin anomaly and deformation/disfigurement (for category descriptions, see Table 1). Occurrence of these features on an individual were noted as a case and the most conclusive frame(s) for identifying the feature(s) were exported and linked to the case. These exported frames were used to quantify the observed features using the free software iTag 0.7 (https://sourceforge.net/projects/itagbiology/) for counting and marking features in images. In addition to these quantifiable features, diatom coverage, i.e., yellowish and brownish skin color, was noted, if evident on the white parts of the body. All information extracted from the sequences was verified by two other persons confirming feature classification. For sequences recorded within a short time interval at the same location, we tried to note possible reappearances of individuals (looking for patterns of conspicuous features that enabled individual identification) to prevent double counts. Aerial footage did not allow for standardized photo identification, for which lateral images of specific parts of the body (blaze, chevron, and dorsal fin) are required (Agler et al., 1990; Whooley et al., 2011). For diagnosis of observed features and identification of possible agents we consulted standard handbooks of marine mammal medicine (e.g., Dierauf & Gulland, 2001) and compared our findings to published literature. Correlation between features was tested using a Pearson correlation test. A total of 109 fin whales were recorded from head to dorsal fin, of which 62 individuals exhibited at least one conspicuous feature. Altogether, 367 individual features were observed across all individuals (Table 2). The most common features were circular white spots (Figure 1; 222 spots found on 51 individual fin whales), followed by dents (Figure 2; 87 dents/20 individuals), scars (Figure 3, Figure 4; 34 scars/24 individuals), and pale patches (Figure 5; 21 patches/13 individuals). Only two cases of deformations of the fin (Figure 6) and one skin anomaly (Figure 7) were detected. 42 fin whales exhibited brownish or yellowish diatom coloring on white parts of the body (Figure 1, Figure 8). The Pearson correlation test of feature categories revealed a positive correlation of circular white spots with dents (r = 0.41), pale patches (r = 0.51) and scars (r = 0.6), and of dents with pale patches (r = 0.28) and scars (r = 0.27), and between pale patches and scars (r = 0.54) (Figure 9). Altogether, the review of body marks revealed little indication for severe impacts on the recorded fin whales. No signs of fresh injuries were detected. The scars detected were mainly small and minor, i.e., not indicative of severe trauma as e.g., inflicted by propellers during ship strikes (Byard et al., 2012; Luksenburg, 2014) or deep cuts caused by fishing gear (Moore, 2014). The largest scar recorded is depicted in Figure 4 and was likely caused by a minor injury of unknown origin. One fin whale had two linear scars on the back, perpendicular to the body axis (Figure 3), which could be indicative of interaction with fishing gear (Luksenburg, 2014). However, the scars suggest superficial abrasions rather than deep cuts. Shapes and locations of all other scars were rather unspecific and did not point to a typical agent such as fishing gear (Luksenburg, 2014; Moore et al., 2013) or predatory scarring (Corsi et al., 2022). In two fin whales the fins were classified as deformed (Figure 6), resembling disfigurement inflicted by fishing gear (Baird & Gorgone, 2005; Kiszka et al., 2008). However, no additional lesions or scars that could have provided additional indication for interaction with fishing gear were associated with either of the malformed fins. From the observed status it is not possible to finally deduce the origin of the deformities, if they were anthropogenic, inflicted by predators or maybe a congenital condition. Altogether, the counts of scars and lesions were low, pointed to minor rather than major previous injury and provided no evidence for entanglement or ship strike. Since aerial imagery has been shown to detect a high share of entanglement scars in rorqual whales (compared to vessel-based photography) (Ramp et al., 2021), we deem it unlikely that major features like entanglement scars and propeller cuts went undetected in our study, particularly given the large number of smallest features that were detected. Examples from cetaceans in human high-use marine areas show a completely different spectrum of injuries and demonstrate that signs of severe trauma can be quite common in cetacean populations (Baird & Gorgone, 2005; Bonneville et al., 2021; Herr et al., 2020; Kiszka et al., 2008). Fin whales are considered to be a predominantly offshore species (Mackintosh & Wheeler, 1929; Perrin et al., 2008). This makes them generally less prone to human impacts, which often occur in coastal areas. However, offshore activities like fishing may still have severe impacts on offshore species, e.g., in terms of interaction during depredation events (Werner et al., 2015), due to entanglement in lost or discarded fishing gear (Stelfox et al., 2016) or offshore shipping traffic (Neilson et al., 2012). Fin whales are among the most regular victims of ship strikes (Laist et al., 2001; Schoeman et al., 2020), with strike rates giving reason for concern e.g., in the heavy traffic area of the Mediterranean (Panigada et al., 2006). Prevalence of scars in fin whales of the Gulf of Maine indicate high rates of entanglement in fishing gear (Ramp et al., 2021). With these observations in mind, the pristine skin conditions of the fin whales gathering at the Antarctic Peninsula suggest that these animals do not migrate to heavily used marine areas after their feeding season in Antarctic waters. If they did, we would expect to see at least some indication for anthropogenic impacts, as is the case in e.g., fin whales from the Mediterranean (Panigada et al., 2006) or in the Gulf of St. Lawrence (Ramp et al., 2021). In addition to the rarity of scars, the complete absence of blister-like skin lesions regularly observed in other large whale populations, e.g., New Zealand blue whales, Balaenoptera musculus (Barlow et al., 2019) and blue, fin and sperm whales, (Physeter macrocephalus) in the Gulf of California (Martinez-Levasseur et al., 2011) is noteworthy. The animals recorded in our study appeared to be in good health, without any signs of severe skin disorders, lesions, or other reasons for concern as far as can be judged from visual inspection. Pale patches were found on 13 individuals. In comparison to the white circular spots, they were generally a bit larger, lighter and more grayish in color, had less defined margins, and not a particular shape. The pale patches occurred ungrouped and were of no specific pattern resembling a skin disease, e.g., tattoo-like lesions (Van Bressem et al., 2015) or poxvirus infections (Geraci et al., 1979; Van Bressem et al., 1999). Histological analyses of pale patches in dolphins have revealed indications of a healing process due to prior trauma, ectoparasite attachment, viral infection, and inflammation (Hart et al., 2012). However, pigmentation anomalies in cetaceans do not necessarily have to be pathogenic. There is natural variation in pigmentation (Alessi et al., 2014; Methion & Diaz Lopez, 2019) and features like the pale patches may also be related to natural skin shedding (Chernova et al., 2016; Reeb et al., 2007). In our study, the etiology of the pale patches remained unknown. However, there was no evidence suggesting an infectious origin. The most frequently detected features in fin whales were small white circular spots (222 spots on 51 individuals; Figure 1). These were detected on different parts of the body in varying numbers per individual (1–14; median 3). All spots were of similar size and shape. They did not resemble typical patterns of a skin disease (Baker, 1992; Bertulli et al., 2012; Kautek et al., 2019) or marks left by barnacles (Félix et al., 2006). Comparison with published documentations of similar spots on other cetaceans suggest that these may be scars from cookiecutter shark (Isistius spp.) bites (Barlow et al., 2019; Dwyer & Visser, 2011; Jones, 1971; Moore et al., 2003). Barlow et al. (2019) describe four healing phases of cookiecutter shark bite lesions in blue whales off New Zealand, of which relatively fresh wounds have subdermal tissue visible as pink (phase 1) or yellowish/brownish (phase 2) lesions, and with phase 3 wounds resembling the white circular spots detected in our study. According to Barlow et al. (2019) phase 3 represents a healed wound leaving behind a bright white scar of ovoid shape that can be smooth or indented—consistent with the circular white spots we found on the fin whales. Phase 4, as described by Barlow et al. (2019), represents a completely healed wound leaving behind a depression with returned pigmentation. This description resembles the dents (n = 87 dent/20 individuals) detected in our fin whales. Additional support for this assumption arises from the close correlation of dents and circular white spots cooccurring on the same individuals (Pearson's r = 0.41). Taking circular white spots and dents into account together, 54 fin whales (49.5%) recorded in our study had cookiecutter shark bite lesions in advanced stages of healing. However, no fresh cookiecutter shark bite lesions were found on fin whales in this study, with neither phase 1 nor phase 2 healing stages present (Barlow et al., 2019). Assuming a regular, seasonal migration of fin whales between temperate waters and the Southern Ocean (Mackintosh, 1966; Mizroch et al., 1984), this indicates a considerably faster healing process than the period of 38 months for progression from phase 2 to phase 3 as found by Barlow et al. (2019) in blue whales based on resighting data. If this were true for fin whales, at least some phase 2 lesions would have to be expected on individuals in Antarctic waters. These were neither described by the whalers, who had the full bodies of whales available for inspection (Mackintosh & Wheeler, 1929). We therefore suggest faster healing in fin whales from the Antarctic Peninsula, with lesions likely reaching phase 3 within one season. This conclusion is further supported by records of cookiecutter shark bites in Antarctic killer whales (Orcinus orca), which are also only present in advanced stages of healing when observed in Antarctic waters and for which maximum healing rates of 150 days between open wound and healed scar have been described (Dwyer & Visser, 2011). The high prevalence of cookiecutter shark bites provides some indication on the migratory origins of the fin whales at the Antarctic Peninsula. Most records of cookiecutter bites on cetaceans are attributed to I. brasiliensis (Best & Photopoulou, 2016; Dwyer & Visser, 2011; Moore et al., 2003), which has a circumpolar, predominantly tropical distribution in offshore waters, mainly between 20°N and 20°S (Ebert, 2003), with the most southerly record from Tasmania at ~41°S (Jahn & Haedrich, 1988) and a distribution in the South Atlantic no further south than 37°S (Best & Photopoulou, 2016). This distribution suggests that at least a share of the fin whales feeding at the Antarctic Peninsula move to an offshore habitat at latitudes lower than 41°S for the breeding season. However, whether all fin whales feeding at the Antarctic Peninsula belong to the same population sharing a common breeding ground remains unknown. Isistius spp. bite marks have been used as a population marker in South Atlantic Bryde's whales (Balaenoptera edeni; Best, 1977; Best & Photopoulou, 2016) and suggested as a marker for a relatively isolated fin whale population around the Cap Verde Islands, based on the fact that other than these fin whales, fin whales from surrounding areas did not have any bite marks (Moore et al., 2003). The presence or absence of bite marks on fin whales at the Antarctic Peninsula could be a population marker indicating mixing of at least two populations on the feeding ground, with only one of them spending the breeding season in waters with a high cookiecutter shark abundance. But this cannot be concluded based on this study and remains speculative. It is similarly possible that some individuals are more susceptible to cookiecutter shark bites than others. To gain more insights into population structure, tracking, and genetic or photo-identification of individuals with and without lesions would be useful for further investigation. In conclusion, our results provide indication that fin whales feeding at the Antarctic Peninsula migrate to an offshore habitat with comparably little human impact, in warm waters within the distributional range of Isistius brasiliensis. We thank the crew of the R/V Polarstern and the helicopter team of expedition PS112 for facilitating our data collection. Special thanks go to the cruise leader Bettina Meyer for supporting our work on board. We are grateful for the help of Rob Hawthorne and Cleone Fox and thank the BBC Seven Worlds, One Planet team. This work was supported by the German Research Foundation (DFG) in the framework of the priority program "Antarctic Research with comparative investigations in Arctic ice areas" SPP 1158 by grant HE 5696/3-1, by the Southern Ocean Research Partnership (IWC-SORP), and by the Antarctic Wildlife Research Fund. Aerial surveys were conducted by permit No. II. 2.8 – 94003-3/408 of the German Environmental Agency in accordance with the Act Implementing the Protocol of Environmental Protection to the Antarctic Treaty (AIEP). Filming was conducted under Permit No. 40/2017 under Section 3 of the Antarctic Act 1994, granted by Polar Regions Department of the Foreign & Commonwealth Office (FCO), UK. Open Access funding enabled and organized by Projekt DEAL. Helena Herr: Conceptualization; data curation; formal analysis; funding acquisition; investigation; methodology; project administration; writing – original draft; writing – review and editing. Sacha Viquerat: Conceptualization; data curation; formal analysis; investigation; methodology; writing – review and editing. Tobias Naujocks: Formal analysis; investigation; methodology; writing – review and editing. Bertie Gregory: Data curation; formal analysis; writing – review and editing. Abigail Lees: Conceptualization; formal analysis; methodology; writing – review and editing. Fredi Devas: Conceptualization; funding acquisition; methodology; project administration; resources; writing – review and editing.