The cookie-cutter shark is the common name for two species of the genus Isistius Gill small sharks of the family Dalatiidae that reach maximum lengths of 56 cm and are distributed throughout pelagic tropical and subtropical waters of all oceans, often being captured between the surface and 3,500-m depths (Ebert, 2013, 2015; Ebert and Stehmann, 2013; Petean, 2014). These sharks feed on large marine animals such as tuna, swordfish, whales, sharks, and dolphins (Dwyer and Visser, 2011, Hoyos-Padilla et al., 2013). Honebrink et al. (2011) even catalog humans as being this fish's potential prey.
The common rorqual, also known as the fin whale, Balaenoptera physalus (Linnaeus) is the second largest living animal, in some cases reaching 27 m in length and weighing up to 75 tons (Shirihai and Jarrett, 2006; Bolaños-Jimenez et al. 2015). Its distribution is cosmopolitan, being observed mainly in temperate and polar seas and coastal and oceanic waters, presenting a seasonal latitudinal migration (Jefferson et al., 1993, Clark and Charif, 1998). This species has been one of the most historically affected by the whaling industry, and its populations have decreased drastically. Therefore, the Convention on International Trade in Endangered Species (CITES, 2014) includes it in Appendix I, and the International Union for Conservation of Nature (IUCN) includes it on the Red List of threatened species (Reilly et al., 2013). It also appears in Annex II of the Protocol on specially protected areas and flora and fauna in the Grand Caribbean Region (SPAW, 1991) and is registered in the Red Book of Venezuelan Wildlife (Bolaños-Jiménez et al., 2015). This cetacean plays an important role in marine ecosystem dynamics, transferring nutrients and energy to trophic levels, being perhaps the most euryphagic of the balaenopterids (Aguilar, 1985). In Venezuela, records of B. physalus are rare, and no estimates exist on their population size (Bolaños-Jiménez et al., 2015).
Marine mammals, primarily odontocetes, frequently become stranded on coasts worldwide (Simmonds, 1997, Bolaños-Jiménez et al., 2014). In Venezuela, between 1988 and 2014, 614 events, affected 23 species, 3 of them involving B. physalus (Bolaños-Jiménez et al., 2014). Although they appear to be seasonal, precise occurrences are unpredictable, making it difficult to generate information on the symbiotic relationships that these mammals maintain.
The stranding of a 19.90-m-long male B. physalus on Isla de Margarita, Venezuela (10°59'32.28" N and 64°23'40.46" W), provided a good opportunity to describe and report interactions between the cookie-cutter shark and the common fin whale. Nearby fishermen observed the cetacean as it approached the coast, providing an early warning to authorities. The stranding was closely monitored and followed until the whale's death and final disposition. The whale was measured and sexed per Smith (2002) and underwent extensive external in situ examinations to determine the presence of adhered macroscopic epithelial organisms and/or macroparasites.
Thirty-three lesions were evidenced along different points of the whale's integument. Other lesions in the underlying areas of the stranded specimen were not ruled out. The wounds were oval or rounded, crater-like, 5 to 7 cm long, 5 to 6 cm wide and 3 to 5 cm deep (Fig. 1A). Approximately 10% of the wounds showed complete remodeling; 60% were more recent but were advancing in dermal repair; and the remaining 30% were very recent and still bleeding (Fig. 1B). The wounds were attributed to the cookie-cutter shark, Isistius sp. (Dalatiidae).
Mackintosh and Wheeler (1929) were the first to describe in detail injuries in B. physalus and B. musculus in subtropical and temperate waters but could not conclude the injuries' source. Jones (1971) linked these injuries to cookie-cutter shark bites. Subsequently, reports of lesions in cetaceans have been attributed to Isistius spp. (Pérez-Zayas et al., 2002; Moore et al., 2003; Dwyer and Visser, 2011; Wenzel and López, 2012; Hoyos-Padilla et al., 2013). Wounds to Isistius spp. have been described by several authors (Mackintosh and Wheeler, 1929; Jones, 1971; Williams and Bunkley-Williams, 1996; Souto et al., 2007; Best and Photopoulou, 2016), coinciding closely with this study's observations in both measurements and morphology.
Isistius is the only shark genus known to maintain parasitic relationships with other organisms (Helfman et al., 2009). Among their adaptations to that lifestyle, cookie-cutter sharks have teeth that are proportionately large for their bodies and are organized closely together. Jones (1971) described that their lips are projected and attached to the surface when biting, forming a seal, and their tongues move backwards due to the well-developed coracohyoid muscles. The spiracles remain closed, forming a large oral cavity that generates a great vacuum, which, coupled with the sharks' great speed and body rotation that imprints upon biting, allows the sharks to extract large conical bites from their hosts (Shirai and Nakaya, 1992; Williams and Bunkley-Williams, 1996; Mota, 2004; Nelson, 2006; Helfman et al., 2009).
Other reported skin affectations in marine organisms are those inflicted by barnacles (Balanidae), lampreys (Petromyzontidae) and remora (Echeneidae). Such interactions were discarded in this case because of the type of wounds generated, clearly distinguishable by their smaller size and shallower depth, among other aspects. Barnacles, such as Coronula sp., produce superficial injuries, and, although embedded in the skin, do not penetrate the epidermis (Mackintosh and Wheeler, 1929) but leave a grayish impression with radially arranged furrows and ridges (Mead et al., 1982). Lampreys usually scrape the integument of fish or cetaceans with their keratinous teeth, feeding on host fluids and generating superficial damage with a characteristic pattern: epidermal abrasion around the suction disk, with a central hole (Williams and Bunkley-Williams, 1996). These authors indicated that lampreys are associated with numerous fish species but rarely with whales, at least in Atlantic waters.
Petromyzon marinus Linnaeus, the only marine species of the group, generally presents an antitropical distribution pattern, that is, it is only found in temperate eastern and western North Atlantic waters (Renaud, 2011). Injuries associated with remora are of low pathological impact and mainly include dermal irritations because they feed mainly on food residue from their hosts, not on the host's tissues (Williams and Bunkley-Williams, 1996).
Other elasmobranches, such as Dalatias licha (Bonaterre), have been recorded in the same geographical area (Tagliafico et al., 2007) and have dimensions (as juveniles) and a dental form that inflict damages similar to those evidenced in this study. However, the feeding habits of this species have been sufficiently studied and consist of various small prey (López Calero, 2013) rather than large marine mammals. No known reference exists in the literature linking D. licha with bites of this type on large marine hosts.
A consensus exists that marine cetaceans are injured by Isistius spp. exclusively in warm waters, so this may provide information on their migration patterns or age (Mackintosh and Wheeler, 1929; Mead et al., 1982; Williams and Bunkley-Williams, 1996). Wounds attributable to Isistius sp. were previously observed in Venezuela on a specimen of Kogia sima stranded alive in the northeastern part of the country in 2001 (Bermúdez-Villapol et al., 2008). All the above strongly indicate the occurrence of facultative Isistius parasitism on B. physalus in Venezuelan waters. Lesions on B. physalus consistent with elasmobranch attacks have been reported in the South Georgia Islands (Mackintosh and Wheeler, 1929), eastern Pacific (Jefferson et al., 1993), Cape Verde Islands (Moore et al., 2003; Wenzel and López, 2012) and South Africa (Best and Photopoulou, 2016). To the authors' knowledge, this is the first reference of this relationship in Venezuelan waters or for the Caribbean and western Atlantic.
Although many studies exist on injuries caused by cookie-cutter sharks, little is known of their magnitude. Best and Photopoulou (2016) reported up to 43 lesions from Isistius sp. on fin whales, which the authors of this report consider to be of high severity. The variability in the lesions' conditions indicates that the interaction between Isistius and B. physalus occurred over a long period (possibly months). This agrees with the parasitic behavior attributed to Isistius in specimens captured or examined live. The most recent lesions might suggest that this elasmobranch was also a scavenger, although in this case, scavenging behavior was unlikely, given that being observed. The foregoing allows us to reasonably affirm that fish of the genus Isistius were responsible for the trauma to the B. physalus stranded in the Macanao peninsula, Isla de Margarita, Venezuela.