Abstract
Skin color aberrations are naturally occurring abnormal pigment patterns that are generally rare among chondrichthyans. In this study, we highlight different skin color aberrations from observations of four shark species native to southern California, USA. We report the first recorded instance of apparent leucism (regional pigmentation loss), in a California horn shark Heterodontus francisci (Girard 1855) and tope shark Galeorhinus galeus (Linnaeus 1758). We also report the apparent second documented occurrence of albinism in the swell shark Cephaloscyllium ventriosum (Garman 1880) from a newly hatched captive individual with parents of normal pigmentation. Lastly, we redescribe a rare secondary color morph in the leopard shark Triakis semifasciata Girard 1855 using previous literature and new sightings/images from sharks in the wild. Color aberrations may lead to different advantages (e.g., certain color morphs may offer additional camouflage) or disadvantages (e.g., reduced pigmentation may limit camouflage and protection from ultraviolet light). Documenting these rare color aberrations augments our understanding of how color patterns can vary between individuals and taxa, and ultimately how these conditions potentially impact shark biology.
Avoid common mistakes on your manuscript.
Skin color aberrations are abnormal skin patterns including conditions leading to excessive pigmentation (i.e., hypermelanosis) or pigment deficiencies (i.e., hypomelanosis) as well as general polymorphism (different color morphs). Skin color aberrations have been attributed to both inheritable homozygous and heterozygous mutations, as well as epigenetic responses to environmental factors including diet, disease, injury, inbreeding, and temperature (Sage 1962; Sandoval-Castillo et al. 2006; Espinal et al. 2016; Gervais et al. 2016). In fishes, there are six identified chromatophores that contribute to skin pigmentation and each produce pigments of varying colors and functions (Bechtel 1995; Bagnara and Matsumoto 2006). Observations of pigment deficiency in chondrichthyans (i.e., sharks, rays, and chimaeras) are overwhelmingly attributed to loss of melanin (Supplemental Table 1), which is responsible for black or brown coloration and is produced within melanophores (Bechtel 1995; Bagnara and Matsumoto 2006). Hypomelanosis, a collective term for all conditions leading to the full (i.e., albinism) or partial (e.g., leucism, piebaldism) loss of melanin pigmentation (Shipley et al. 2023), is quite rare in chondrichthyans and has only been described in < 5% of chondrichthyan species (69 of the 1483 identified species) (Fricke et al. 2023; Supplemental Table 1). Albinism is a genetic condition in which the individual completely lacks the ability to produce melanin, typically resulting in completely white skin and often red irises of the eyes (Clark 2002; Sandoval-Castillo et al. 2006; Bigman et al. 2016). Leucism, or partial albinism, is the term for a broad suite of conditions in which the individual can still produce pigmentation but lacks melanin across certain regions of the body where melanin is typically present (Berdeen and Otis 2011; Bigman et al. 2016; Wargat et al. 2023). Leucistic sharks often retain normal-colored eyes (Clark 2002; Bigman et al. 2016; Arronte et al 2022). In addition to conditions that affect pigment production, skin color aberrations can include uncommon color morphs, in which individuals of a single species exhibit distinct color patterns. In fish species that exhibit color polymorphism, color morphs can vary with sex, time (ontogenetic or seasonal changes), and habitat (Gray et al. 2008; Korzan et al. 2008; Maan and Sefc 2013; Dahl et al. 2019).
Here, we document macroscopic observations of irregular skin patterns in four shark species native to the coast of southern California, USA. We report an apparent case of leucism in the California horn shark Heterodontus francisci (Girard 1855) made from four separate observations of the same individual in the wild between 2019 and 2023. In addition, we report an apparent case of leucism within the tope shark Galeorhines galeus (Linnaeus 1758) from a chance encounter in the wild in 2023. We also report an apparent case of albinism in the swell shark Cephaloscyllium ventriosum (Garman 1880) from a captive individual in 2019. Lastly, we report additional observations of an anomalous color pattern in the leopard shark Triakis semifasciata Girard 1855 made from various observations. While this secondary color morph has previously been documented by Schott (1964) and Castro (2011), we provide unique images of these individuals in the wild and discuss this trait in context of historical sightings.
Leucism in the California horn shark
Here we report four independent sightings of a male California horn shark with apparent leucism from the coastal waters of La Jolla, CA, across a 4-year time span (Fig. 1). This individual had a blotchy complexion, with the apparent lack of skin pigmentation in various regions, while maintaining normal eye pigmentation. This same individual, identified by its distinct pigmentation patterns, was observed on four confirmed occasions: (1) resting in the rocky reef habitat of La Jolla Cove along with normally pigmented horn shark individuals (Fig. 1A–C, daylight hours, May 9, 2019, approximately 32.851 N, 117.266 W); (2) approximately 2 km northwards over a sandy bottom near Scripps Institution of Oceanography pier (Fig. 1D, night time hours, June 24, 2019, 32.867 N, 117.257 W); (3) in La Jolla Cove (Fig. 1E, daylight hours, June 18, 2020, exact coordinates not provided); and (4) among normal pigmented conspecifics in the rocky reefs of La Jolla Cove less than 0.5 km from the first sighting (Fig. 1F, Supplemental Videos 1 and 2, daylight hours, April 6, 2023, 32.851 N, 117.270 W). The shark was briefly retained on the June 2019 encounter during the collection of other horn sharks for non-related work (Prinzing et al. 2021, 2023) and estimated to be between 55 and 60 cm total length. This is the first record of a California horn shark with apparent leucism and the second Heterodontus species (out of nine) with a documented case of hypomelanosis. A unique case of leucism has previously been reported in the closely related Port Jackson shark H. portjacksoni (Meyer 1793) from Australia, although this individual still appeared to produce yellow pigmentation (Jha 2004; The Sydney Morning Herald 2004; Veena et al. 2011).
Hypomelanosis often leads to certain biological disadvantages including lack of protection from ultraviolet rays and increased risk of predation due to the conspicuous nature of a white body against the contrasting environmental background. This may ultimately reduce animal survival and further contribute to the rare observation of hypomelanosis in the wild (Uieda 2000; Sandoval-Castillo et al. 2006; Acevedo et al. 2009). However, our multiple observations of the mature horn shark over several years suggests that leucism may not adversely affect its health and survival. Horn sharks generally seek shelter in rocky crevices during the day, when a hypomelanistic individual would be most conspicuous to predators, and then feed at night when a lack of skin pigmentation would be of less concern (Nelson and Johnson 1970; Strong 1989; Meese and Lowe 2020a; Meese and Lowe 2020b). Horn sharks also exhibit high site fidelity and often return to the same feeding grounds and resting places (Strong 1989; Meese and Lowe 2020a, 2020b), which in this case has allowed for multiple observations and unique insight into the continued health and survival of this leucistic individual.
Leucism in the tope shark
On August 6, 2023, an adult tope shark with apparent leucism was observed swimming within La Jolla Cove, CA (32.850 N, 117.266 W), above a shallow rocky reef (Fig. 2), among an aggregation of conspecifics characterized as mostly pregnant females (Nosal et al. 2021). The individual exhibited typical gray pigmentation with a noticeable blotch of non-pigmented skin between the first and second dorsal fin on the right lateral body and had normal-colored eyes. Hypomelanosis in the form of albinism has been reported twice before from two tope individuals caught in the north Atlantic Ocean (Deynat 2003; Quigley et al. 2018), but this represents the first report of apparent leucism within the species, and the first reported individual with hypomelanosis within the Pacific Ocean. While topes are found circumglobally in coastal temperate waters, there is little to no gene flow between populations or oceans (Chabot and Allen 2009; Chabot 2015).
Albinism in the swell shark
In December 2019 at Scripps Institution of Oceanography, a swell shark lacking any skin pigmentation (Fig. 3) hatched from an egg laid by a captive female with normal pigmentation. This is the second known observation of apparent albinism in this species. The other known instance of albinism in swell sharks is from a mature female caught near Cabo San Lucas, Baja California Sur, Mexico, in 2016 (Becerril-García et al. 2017). While in many species, including chondrichthyans, albino individuals are often characterized by red eyes (Reum et al. 2008; Lipej et al. 2011), both known albinistic swell shark individuals appeared to have normal-colored eyes, likely attributed to the presence of chrysopsin and rhodopsin pigments, both of which would not be affected by changes to melanin production as they are produced by different enzymes in different chromatophores (Denton and Warren 1956; Crescitelli et al. 1985; Crescitelli 1991; Wang et al. 2007; Becerril-García et al. 2017).
Secondary color morph in the leopard shark
Lastly, we document additional cases of an anomalous color pattern in leopard sharks (Fig. 4; Table 1). This species’ primary color morph (initially called “primary chromatic pattern” by Schott (1964) and included in the original species descriptions as referenced in Pietsch et al. (2012)) is characterized by small spot marks and larger dark saddle bars that straddle the dorsal and lateral surface of the shark (Fig. 4A). In contrast, a separate, anomalous pattern (first introduced as a “secondary chromatic pattern” by Schott (1964)), is characterized by more irregular saddle bars with strong longitudinal marks, concave indents, or branches, and often accompanied by smaller and numerous irregular marks and spots extending laterally along the sides of the shark (Fig. 4B–D; Schott 1964; Castro 2011). These irregular patterns and longitudinal streaks have resulted in nicknames for this color morph such as “scribbled,” “tire treads,” or “zig zags” (personal observations) and are easy to identify when compared with individuals with the primary color morph (Fig. 4E–F). To be consistent and avoid confusion moving forward, we suggest that this anomalous pattern in leopard sharks be referred to as the “secondary” color morph. While most sharks appear to group within one of these two descriptions, it is important to note that there is large variation in both the primary and secondary color morphs. Specifically, the number, size, and placement of both saddles and spots can vary in both morphs and the shape of the secondary marks can vary greatly in the secondary color morph. Thus, it is possible these morphs could be further divided into more distinct sub-groupings or viewed as a graded spectrum between the two morphs, although more in-depth demographic research would be needed to discern these scenarios.
Here, we report 11 additional observations of the secondary color morph to the original reports by Schott (1964) and Castro (2011). These observations were collected from various sources including our own in situ observations (Fig. 4A–C, E–F), and information we collated from online posts (i.e., videos and blog articles by fishermen and outdoor enthusiasts), and from captive individuals located at the Birch Aquarium (Fig. 4D) and the Living Coast Discovery Center (Table 1). Included in our observations were five individuals observed at a local female aggregation site in La Jolla, California. Combining our new dataset with rare historical records (Table 1), this secondary color morph has now been documented across a 76-year time span encompassing regions from Goleta, California, USA, to San Quintin Bay, Baja California, Mexico (over 350 miles apart), including the offshore Channel Islands. Considering leopard sharks live upwards of 25–30 years (Smith 1984; Kusher et al. 1992; Smith et al. 2003), this represents at least three generations of individuals with this color morph, indicating its persistence as a rare, but regularly encountered trait.
The driving mechanism behind these divergent color morphs and their relative proportion is not known. Of the 150 individuals that Schott (1964) sampled (n = 49), observed (n = 100), or mentioned via personal communication (n = 1), three individuals (2%) were of the secondary color morph. While it is possible that this is simply a rare genetic mutation with little biological significance, Dahl et al. (2019) hypothesized the “sandy” color morph for the Zebra Shark Stegostoma tigrinum (Forster 1781), a species known for its variegated patterns similar to the leopard shark, may provide camouflage advantages for individuals inhabiting sandy habitats. Leopard sharks are known to occupy a wide variety of habitats including sandy flats, eelgrass beds, and rocky reefs (Ebert 2003; Castro 2011), in which different color morphs could potentially provide some benefit. Although we observed both color morphs over both rocky reefs and sandy flats, a larger sample size and a more exhaustive survey of leopard shark color morph demography and habitat use would be needed to understand any potential correlations between a specific morph and habitat type. Interestingly, we were unable to find documented reports of the secondary color morph from leopard sharks north of Point Conception, CA, which is a known barrier to gene flow between leopard shark populations to the north and south (Barker et al. 2015), although this could simply reflect underreporting in northern areas where there are fewer interactions with leopard sharks.
Implications
Similar to other documented instances of hypomelanosis and rare color morphs, this paper is based on chance observations rather than a directed study of the topic. Thus, our results and those of other papers on skin aberrations generally suffer from a few challenges. First, due to the rarity of encounters, chance observations do not allow for a clear understanding of the prevalence and variation of color aberrations within and between species. Second, because observations of skin conditions are mostly described from external color alone, the underlying physiological (e.g., lack of pigment production, lack of melanocytes) and genetic causes are generally not assessed. For example, of the 84 studies listed in Table S1 documenting chondrichthyan hypomelanosis, only one study (Wargat et al. 2023) included histological examination to show that the described leucism in this animal was caused by a loss of melanin in the skin. Histological and genetic testing can thus be used to discern specific causes in rare cases in which skin aberrations occur in captivity or in wild animals that are captured and retained. While most skin aberrations are thought to fall under the umbrella of hypomelanosis, there are other chromatophores and pigments that contribute to coloration, and it is often unclear to what extent those chromatophores and pigments play a role. Finally, it is also possible that such encounters may go unreported in the literature due to the topical nature of the subject or because it may not be broadly known how atypical these occurrences are. As an example, we falsely assumed that hypomelanosis had been previously recorded in California horn sharks, and it took us four years before we realized this was a unique observation. Examining individuals with skin aberrations in captivity also provides a rare opportunity to further study the genetics and inheritance of such traits. For instance, mating between a male and female of known phenotypes can allow for studies of inheritance in pups born in captivity. Thus, due to their rarity, it is important to document both wild and captive observations of skin aberrations in order to help understand color patterns and their biological significance across time, space, and taxa, and to help inform future observations.
Data availability
All data is provided within the manuscript and supplementary material.
Data accessibility
Raw picture and videos files are available at https://figshare.com/s/88dba2835756b69def9a.
References
Acevedo J, Aguayo-Lobo A, Torres D (2009) Albino weddell seal at cape shirreff, Livingston island, Antarctica. Polar Biol 32:1239–1243. https://doi.org/10.1007/s00300-009-0680-8
Ari C (2014) Rapid coloration changes of manta rays (Mobulidae). Biol J Lin Soc 113(1):180–193. https://doi.org/10.1111/bij.12321
Arronte JC, Antolínez A, Bañón R, Rodríguez-Gutiérrez J, Ortíz JJ, Martínez JM (2022) First recorded case of leucism in the velvet belly lantern shark Etmopterus spinax (Squaliformes: Etmopteridae). J Appl Ichthyol 38(4):455–461. https://doi.org/10.1111/jai.14326
Bagnara JT, Matsumoto J (2006) Comparative anatomy and physiology of pigment cells in nonmammalian tissues. In: Nordlund JJ, Boissy RE, Hearing VJ, King RA, Ortonne JP (eds) The Pigmentary System: Physiology and Pathophysiology. Oxford University Press, New York, pp 9–40
Barker AM, Nosal AP, Lewallen EA, Burton RS (2015) Genetic structure of leopard shark (Triakis semifasciata) populations along the Pacific coast of North America. J Exp Mar Biol Ecol 472:151–157. https://doi.org/10.1016/j.jembe.2015.06.020
Becerril-García EE, Tamburin E, González-Armas R, GalvánMagaña F (2017) First record of albinism in the swell shark, Cephaloscyllium ventriosum (Elasmobranchii: Carcharhiniformes:Scyliorhinidae). Acta Ichthyol Piscat 47(2):201–204. https://doi.org/10.3750/AIEP/02175
Bechtel HB (1995) Reptile and amphibian variants: colors, patterns, and scales. Krieger Publishing Co., Melbourne, Florida
Berdeen JB, Otis DL (2011) An observation of a partially albinistic Zenaida macroura (mourning dove). Southeast Nat 10(1):185–188. https://doi.org/10.1656/058.010.0117
Bigman JS, Knuckey JDS, Ebert DA (2016) Color aberrations in Chondrichthyan fishes: first records in the genus Bathyraja (Chondrichthyes: Rajiformes: Arhynchobatidae). Mar Biodivers 46:579–587. https://doi.org/10.1007/s12526-015-0403-z
Castro JI (2011) The sharks of North America. Oxford University Press, Oxford, United Kingdom
Chabot CL (2015) Microsatellite loci confirm a lack of population connectivity among globally distributed populations of the tope shark Galeorhinus galeus (Triakidae). J Fish Biol 87(2):371–385. https://doi.org/10.1111/jfb.12727
Chabot CL, Allen LG (2009) Global population structure of the tope (Galeorhinus galeus) inferred by mitochondrial control region sequence data. Mol Ecol 18(3):545–552. https://doi.org/10.1111/j.1365-294X.2008.04047.x
Clark S (2002) First report of albinism in the white-spotted bamboo shark, Chiloscyllium plagiosum (Orectolobiformes: Hemiscyllidae), with a review of reported color aberrations in elasmobranchs. Zoo Biol: Published in Affiliation with the American Zoo and Aquarium Association 21(6):519–524. https://doi.org/10.1002/zoo.10068
Crescitelli F (1991) The natural history of visual pigments: 1990. Prog Retin Res 11:1–32. https://doi.org/10.1016/0278-4327(91)90022-T
Crescitelli F, McFall-Ngai M, Horwitz J (1985) The visual pigment sensitivity hypothesis: further evidence from fishes of varying habitats. J Comp Physiol A 157:323–333. https://doi.org/10.1007/BF00618122
Dahl RB, Sigsgaard EE, Mwangi G, Thomsen PF, Jørgensen RD, de Oliveira TF, Olsen L, Møller PR (2019) The sandy zebra shark: a new color morph of the zebra shark Stegostoma tigrinum, with a redescription of the species and a revision of its nomenclature. Copeia 107(3):524–541. https://doi.org/10.1643/CG-18-115
Denton EJ, Warren FJ (1956) Visual pigments of deep-sea fish. Nature 178:1059–1059
Deynat PP (2003) Albinisme partiel chez le pailona commun, Centroscymnus coelolepis (Elasmobranchii, Somniosidae). Cybium 27(3):233–236. https://doi.org/10.26028/cybium/2004-273-006
Domeier ML, Nasby-Lucas N (2007) Annual re-sightings of photographically identified white sharks (Carcharodon carcharias) at an eastern Pacific aggregation site (Guadalupe Island, Mexico). Mar Biol 150:977–984. https://doi.org/10.1007/s00227-006-0380-7
Dudgeon CL, Noad MJ, Lanyon JM (2008) Abundance and demography of a seasonal aggregation of zebra sharks Stegostoma fasciatum. Mar Ecol Prog Ser 368:269–281. https://doi.org/10.3354/meps07581
Ebert D (2003) Sharks, rays, and chimaeras of California. University of California Press, California
Espinal M, Mora JM, Ruedas LA, López LI, Marineros L (2016) A case of albinism in the Central American spider monkey, Ateles geoffroyi. Honduras Mastozoología Neotropical 23(1):63–69
Fricke R, Eschmeyer WN, van der Laan R (eds) (2023) Eschmeyer’s Catalog of Fishes: Species by Family/Subfamily. http://researcharchive.calacademy.org/research/ichthyology/catalog/fishcatmain.asp Accessed 15 November 2023
Gervais C, Mourier J, Rummer JL (2016) Developing in warm water: irregular colouration and patterns of a neonate elasmobranch. Mar Biodivers 46:743–744. https://doi.org/10.1007/s12526-015-0429-2
Gray SM, Dill LM, Tantu FY, Loew ER, Herder F, McKinnon JS (2008) Environment-contingent sexual selection in a colour polymorphic fish. Proc Royal Soc b: Biol Sci 275(1644):1785–1791. https://doi.org/10.1098/rspb.2008.0283
Jha A (2004) What’s so special about a yellow shark? The Guardian. https://www.theguardian.com/science/2004/apr/01/thisweekssciencequestions1 Accessed on 21 May 2023
Korzan WJ, Robison RR, Zhao S, Fernald RD (2008) Color change as a potential behavioral strategy. Horm Behav 54(3):463–470. https://doi.org/10.1016/j.yhbeh.2008.05.006
Kusher DI, Smith SE, Cailliet GM (1992) Validated age and growth of the leopard shark, Triakis semifasciata, with comments on reproduction. Environ Biol Fishes 35:187–203. https://doi.org/10.1007/BF00002193
Lipej L, Mavrič B, Žiža V, Capapé C (2011) First cases of albinism recorded in the marble electric ray Torpedo marmorata (Chondrichthyes: Torpedinidae). Cahiers de Biologie Marine 52(3):261–267. https://doi.org/10.21411/CBM.A.D22636AD
Lowe C, Goodman-Lowe G (1996) Suntanning in hammerhead sharks. Nature 383(6602):677–677. https://doi.org/10.1038/383677a0
Maan ME, Sefc KM (2013) Colour variation in cichlid fish: developmental mechanisms, selective pressures and evolutionary consequences. Semin Cell Dev Biol 24(6–7):516–528. https://doi.org/10.1016/j.semcdb.2013.05.003
Meese EN, Lowe CG (2020a) Environmental effects on daytime sheltering behaviours of California horn sharks (Heterodontus francisci). Environ Biol Fishes 103:703–717. https://doi.org/10.1007/s10641-020-00977-6
Meese EN, Lowe CG (2020b) Active acoustic telemetry tracking and tri-axial accelerometers reveal fine-scale movement strategies of a non-obligate ram ventilator. Mov Ecol 8:1–17. https://doi.org/10.1186/s40462-020-0191-3
Nelson DR, Johnson RH (1970) Diel activity rhythms in the nocturnal, bottom-dwelling sharks, Heterodontus francisci and Cephaloscyllium ventriosum. Copeia 1970:732–739. https://doi.org/10.2307/1442315
Nosal AP, Cartamil DP, Ammann AJ, Bellquist LF, Ben-Aderet NJ, Blincow KM, Burns ES, Chapman ED, Freedman RM, Klimley AP, Logan RK (2021) Triennial migration and philopatry in the critically endangered soupfin shark Galeorhinus galeus. J Appl Ecol 58(8):1570–1582. https://doi.org/10.1111/1365-2664.13848
Pietsch TW, Orr JW (2012) Eschmeyer WN (2012) Mustelus felis Ayres, 1854, a senior synonym of the Leopard Shark, Triakis semifasciata Girard, 1855 (Carchariniformes: Triakidae), invalidated by “reversal of precedence.” Copeia 1:98–99. https://doi.org/10.1643/CI-11-089
Prinzing TS, Zhang Y, Wegner NC, Dulvy NK (2021) Analytical methods matter too: establishing a framework for estimating maximum metabolic rate for fishes. Ecol Evol 11(15):9987–10003. https://doi.org/10.1002/ece3.7732
Prinzing TS, Bigman JS, Skelton ZR, Dulvy NK, Wegner NC (2023) The allometric scaling of oxygen supply and demand in the California horn shark, Heterodontus francisci. J Exp Biol 226(15):jeb246054. https://doi.org/10.1242/jeb.246054
Quigley DTG, MacGabhann D, Duane P (2018) Albino and leucistic sharks (Elasmobranchii: Selachii) from Irish and British waters: lesser spotted dogfish Scyliorhinus canicula (L.), greater spotted dogfish S. stellaris (L.), spurdog Squalus acanthias L. and tope Galeorhinus galeus (L.). Irish Nat J 36(1):63–66
Reum JCP, Paulsen CE, Pietsch TW, Parker-Stetter SL (2008) First record of an albino Chimaeriform fish, Hydrolagus Colliei. Northwest Nat 89(1):60–62. https://doi.org/10.1898/1051-1733(2008)89[60:FROAAC]2.0.CO;2
Robbins R, Fox A (2012) Further evidence of pigmentation change in white sharks. Carcharodon Carcharias Mar Freshw Res 63(12):1215–1217. https://doi.org/10.1071/MF12208
Sage BL (1962) Albinism and melanism in birds. Br Birds 55(6):201–225
Sandoval-Castillo J, Mariano-Melendez E, Villavicencio-Garayzar C (2006) New records of albinism in two elasmobranchs: the tiger shark Galeocerdo cuvier and the giant electric ray Narcine entemedor. Cybium 30:191–192
Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B, Tinevez JY (2012) Fiji: An open-source platform for biological-image analysis. Nat Methods 9:676–682. https://doi.org/10.1038/nmeth.2019
Schott JW (1964) Chromatic patterns of the leopard shark, Triakis semifasciata Girard. Calif Fish Game 50(2):207–214
Shipley ON, Fitzgerald J, Horne B, Crowe S, Gallagher AJ (2023) Observations of hypomelanosis in the nurse shark Ginglymostoma cirratum. J Fish Biol 102(1):287–289. https://doi.org/10.1111/jfb.15238
Smith SE (1984) Timing of vertebral-band deposition in tetracycline-injected leopard sharks. Trans Am Fish Soc 113(3):308–313. https://doi.org/10.1577/1548-8659(1984)113%3c308:TOVDIT%3e2.0.CO;2
Smith SE, Mitchell RA, Fuller D (2003) Age-validation of a leopard shark (Triakis semifasciata) recaptured after 20 years. Fish Bull 101:194–198
Strong Jr WR (1989) Behavioural ecology of horn sharks, Heterodontus francisci, at Santa Catalina Island, California, with emphasis on patterns of space utilization (Masters thesis). California State University, Long Beach. https://www.proquest.com/openview/17ed950e4fe6a05c8753eeba21a514fa/1?pq-origsite=gscholarandcbl=18750anddiss=y. Accessed 17 May 2023
The Sydney Morning Herald (2004) Yellow shark one in a million. Australian Associated Press. https://www.smh.com.au/national/yellow-shark-one-in-a-million-20040330-gdin0b.html Accessed on 21 May 2023
Uieda W (2000) A review of complete albinism in bats with five new cases from Brazil. Acta Chiropterologica 2(1):97–105
Veena S, Thomas S, Raje SG, Durgekar R (2011) Case of leucism in the spadenose shark, Scoliodon laticaudus (Müller and Henle, 1838) from Mangalore, Karnataka. Indian J Fish 58(1):109–112
Wang J, Hou L, Zhang R, Zhao X, Jiang L, Sun W, An J, Li X (2007) The tyrosinase gene family and albinism in fish. Chin J Oceanol Limnol 25(2):191–198. https://doi.org/10.1007/s00343-007-0191-9
Wargat BN, Adams DH, Habegger ML (2023) Leucism in sharks: a histological examination. J Fish Biol 103(3):731–734. https://doi.org/10.1111/jfb.15431
Acknowledgements
Thank you to Josh Gailey, Alma Trinidad Javier, Ralph Pace, Kevin Smith, and Jordann Tomasek for providing photos for the manuscript. Also thank you to Melissa Torres and Jennifer Moffatt of the Birch Aquarium and Aidan, Kate, and Aiyana Reissman at the Living Coast Discovery Center for providing additional photos and information on their respective leopard sharks. Horn shark observations were made while T.P. and Z.S. were graduate students conducting research supported by Nick Dulvy (Simon Fraser University) and Phil Hastings (Scripps Institution of Oceanography, University of California, San Diego).
Funding
PADI Foundation (grant no. 40569) funded the dive equipment used in this study.
Author information
Authors and Affiliations
Contributions
Contributed to conception and design: Z.R.S.
Contributed to acquisition of data: Z.R.S., T.S.P., Z.V., P.D., A.P.N., P.J.Z.
Contributed to analysis and interpretation of data: Z.R.S., A.P.N., N.C.W.
Edited and approved the submitted version for publication: All authors.
Corresponding authors
Ethics declarations
Ethical approval
The results of this study are from field observations and thus no ethical approval was required. However, the brief handling of the leucistic horn shark during collection of horn sharks for other studies (Prinzing et al. 2021, 2023) was approved by the Institutional Animal Care and Use Committees of the University of California, San Diego (protocol no. S00080) and National Oceanic and Atmospheric Administration Southwest Fisheries Science Center (protocol no. SW1801) and in accordance with California Fish and Wildlife Scientific Collecting Permit SC-13908.
Competing interests
The authors declare no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
About this article
Cite this article
Skelton, Z.R., Prinzing, T.S., Nosal, A.P. et al. Observations of skin color aberrations in four shark species off the coast of southern California, USA. Environ Biol Fish 107, 391–400 (2024). https://doi.org/10.1007/s10641-024-01532-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10641-024-01532-3