A classification system for wounds and scars observed on white sharks (Carcharodon carcharias)

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Introduction The study of large marine organisms is limited due to the difficulty of making field observations throughout the expansive, deep and relatively opaque ocean environment. While significant advances in electronic tagging and molecular techniques have broadened the scope of questions that can be effectively addressed, major aspects of life history remain unknown. White sharks (Carcharodon carcharias) in central California, for instance, are one of the most studied elasmobranch species with over 21,000 instrumented tracking days (Andrzejaczek et al., 2022), documented regional population trends (Kanive et al., 2021), and a sequenced genome (Marra et al., 2019). Despite decades of dedicated research, targeted tourism, and natural history observation (Jorgensen et al., 2022), significant gaps remain in our basic knowledge of their natural history – for example, no one knows the gestation period of a white shark, where they give birth, when and where they mate, and how they interact with prey, predators and each other (Jorgensen et al., 2022). Over the course of these efforts, a proliferation of photographic devices with increasing miniaturization and ever-improving picture resolution has resulted in vast image libraries documenting individual white sharks repeatedly photographed over decades (Anderson et al., 2011). Our observations of white sharks off Central California, documented in an image library, reveal a large number of injuries, wounds, and scars that occur and heal at regular intervals. The unique patterns and the timing of these marks may provide novel insights into the life history of white sharks that have remained undescribed. Additionally, similar libraries from other regional populations (e.g., PHOTO ID citations) can provide insights into region specific as well as broad comparisons of life history patterns. However, before we can use these scars to better understand white shark life history, the source of the wounds must first be determined and systematically classified.To date, a modest number of studies focused on wounds or scars on sharks and marine mammals have made progress in identifying their causes. Injuries resulting from boat strikes and subsequent healing rates have been described on white sharks (Towner et al., 2012) as well as whale sharks (Speed et al., 2008) and manta rays (McGregor et al., 2019). Diagnostic wounds made by propeller blades are reflected by sets of evenly spaced parallel cuts approximately perpendicular to the direction of vessel travel (Rommel et al., 2007; Towner et al., 2012). Scarring on white sharks consistent with interaction with large squid have also been reported (Becerril-García et al., 2020). Squid marks bear a distinctive pattern with rows of circular scars tapering in diameter consistent with suckers ringed with sharp teeth, that flank the arms and tentacles of larger squid species. Small bites extracted by cookiecutter sharks, common on open ocean cetaceans, have also been identified on white sharks (Hoyos-Padilla et al., 2013). Killer whales are a known white shark predator (Jorgensen et al. 2019), and a failed predatory attempt can leave the signature impression of their tightly spaced pointed teeth (De Maddalena 2023).In this paper we propose a systematic classification system to describe the different types of wounds and scars commonly observed on white sharks in the northeastern Pacific associated with prey handling, parasites, conspecific aggression and anthropogenic impacts. The systematic approach described in this study includes a dichotomous key for more efficient and consistent scar classification which may be applicable to numerous other marine organisms where long-term image documentation is obtainable.MethodsFrom 1987 to 2024, while conducting seasonal research on white sharks (Carcharodon carcharias) around seal rookeries in central California (Año Nuevo Island, Southeast Farallon Island, Point Reyes, Tomales Point, and Monterey Bay), we archived hundreds of hours of underwater video recordings of individual sharks (Anderson et al., 2011; Chapple et al., 2011; Kanive et al., 2015, 2019). White sharks were attracted toward our research boat using a seal decoy made from outdoor carpet and deployed with a standard medium tackle rod and reel. In most cases a small (~2kg) piece of marine mammal blubber (use permitted by National Marine Fisheries Service) was tethered to the boat to provide a localized olfactory attractant to increase the shark’s proximity to the boat once they approached. In Monterey Bay, no decoy or attractant was used, sharks were visually spotted at the surface and approached. With the shark near the boat, we recorded video images using a ‘dip camera’ attached to a 2-4 m pole (camera specifications varied over this period but should not impact the results of this study). Whenever possible, both sides of the shark were imaged, with special attention given to the dorsal fin profile, for individual identification, and the rear ventral area, to determine sex (Anderson et al., 2011). While individual ID and sex were initially the primary reason for video documentation, many different types of wounds and scars on the white sharks were recorded. To systematically classify the various scars and wounds, we reviewed a selection of clear scar images and matched the wound impressions with candidate causes based on known interactions classes that could result in injury, these included, 1) Conspecific - e.g. these were aggressive bites or mating hold bites, 2) Prey handling - e.g. scratches or bites from their preferred pinniped prey, 3) Environmental – e.g. scrapes from contact with rocky reef, 4) Parasitic - e.g. cookiecutter shark bites or copepod attachment, and 5) Anthropogenic - e.g. gear entanglement or boat strikes. To facilitate standardizing scar classification, we developed a dichotomous key based on a series of yes/no questions about the size, depth and pattern of an observed wound or scar.Scar categoriesBetween 1987 and 2022 we recorded over 2500 video clips documenting more than 500 unique individual white sharks in central California. Reviewing every scar was beyond the scope of this study, however from a representative collection of scar observations across a range of age, sex, and locations our sorting by similar scar and wound shapes resulted in 12 observed injury sources, each falling under one of the following five broad interaction classes.1ConspecificThe impression of white shark teeth is highly distinctive. Their teeth are serrated, extremely sharp, and are capable of inflicting deep cuts that generally form a crescent shape wound where individual tooth cuts are evenly spaced. If the bite is deeper, the individual tooth impressions connect into a single large and slightly jagged crescent cut. 1.1Mating Hold Bites (Shallow Bites)Many scars and wounds clearly formed the crescent shape impression of a second white shark’s jaw. These scars generally fell into two categories; deep injurious bites, or multiple shallow tooth impressions. Lighter tooth impressions were often repeated in proximity resembling multiple light bites, consistent with a ‘hold’ that was repeatedly adjusted. We categorized these as a ‘Hold Bite’. Similar wound patterns have been identified in other species such as nurse sharks (Gangliocytoma cirratum), blacktip reef sharks (Carcharhinus melanopterus) associated with mating activity (Pratt and Carrier, 2001). 1.2Deep BitesThese bites are typically large and deep where the individual tooth impressions are connected in a continuous crescent shape (Figure 1). These scars can run all the way down the side of the shark, often affecting the gills. What distinguishes these from ‘Hold Bites’ is the depth of the bite and the connected laceration between individual tooth impressions. Unlike Hold Bites, which appear light with multiple repetitions, the Deep Bites appear as one or more single impression deep into the muscle. Whereas Hold

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