Ontogenetic Patterns of Elemental Tracers in the Vertebrae Cartilage of Coastal and Oceanic Sharks

Abstract

As predators, coastal and oceanic sharks play critical roles in shaping ecosystem structure and function, but most shark species are highly susceptible to population declines. Effective management of vulnerable shark populations requires knowledge of species-specific movement and habitat use patterns. Since sharks are often highly mobile and long-lived, tracking their habitat use patterns over large spatiotemporal scales is challenging. However, the analysis of elemental tracers in vertebral cartilage can describe a continuous record of the life history of an individual from birth to death. This study examined trace elements (Li, Mg, Mn, Zn, Sr, and Ba) along vertebral transects of five shark species with unique life histories. From most freshwater-associated to most oceanic, these species include Bull Sharks (Carcharhinus leucas), Bonnethead Sharks (Sphyrna tiburo), Blacktip Sharks (Carcharhinus limbatus), Spinner Sharks (Carcharhinus brevipinna), and Shortfin Mako Sharks (Isurus oxyrinchus). Element concentrations were compared across life stages (young-of-the-year, early juvenile, late juvenile, and adult) to infer species-specific ontogenetic patterns of habitat use and movement. Many of the observed elemental patterns could be explained by known life history traits: C. leucas exhibited clear ontogenetic changes in elemental composition matching expected changes in their use of freshwater habitats over time. S. tiburo elemental composition did not differ across ontogeny, suggesting residence in estuarine/coastal regions. The patterns of elemental composition were strikingly similar between C. brevipinna and C. limbatus, suggesting they co-occur in similar habitats across ontogeny. I. oxyrinchus elemental composition was stable over time, but some ontogenetic shifts occurred that may be due to changes in migration patterns with maturation. The results presented in this study enhance our understanding of the habitat use and movement patterns of coastal and oceanic sharks, and highlights the applicability of vertebral chemistry as a tool for characterizing shark life history traits.

Chemical signatures in fin spine edge of Atlantic bluefin tuna (Thunnus thynnus) can serve as habitat markers of geographically distinct marine environments

“…Mn and Li concentrations were also effective at discriminating ABFT between Atlantic and Mediterranean regions with higher concentrations in tunas collected in the Mediterranean waters. Despite the importance of Mn and Li in this study, the relationship between the environmental concentrations of these elements and their incorporation into calcified structures remains inconsistent across species and environments (e.g., Bath Martin and Thorrold 2005 ; Miller 2009 ; Sturrock et al., 2015 ; Mohan et al., 2018 ; Reis-Santos et al., 2018 ; Livernois et al., 2021 ; Martino et al., 2021 ). In addition, experimental studies did not find any evidence of a relationship between seawater Mn and Mn in otoliths (see review by Miller, 2009 ).…”

“…Sr and Ba were unexpectedly less effective than other elements at discriminating specimens between regions. Sr and Ba uptake in otoliths and fin rays is considered to be an environmental proxy for salinity ( McMillan et al., 2017 ; Livernois et al., 2021 ), and has therefore been used to reconstruct fish migrations across salinity gradients (e.g., Elsdon et al., 2008 ; Allen et al., 2009 ; Avigliano and Volpedo 2013 ; Izzo et al., 2018 ; Rogers et al., 2019 ). In elasmobranch vertebrae, while Sr increases Ba decreases with increasing salinity ( Dorval et al., 2005 ).…”

“…The tracer element and stable isotopic composition of biomineralized structures, including otoliths (ear stones), fin spines, rays, vertebrae, and scales, can add valuable knowledge of seawater conditions in which these chemical markers were deposited. Biomineral chemical markers thus represent a powerful tool for understanding the movement, population structure, and habitat use of fish species (e.g., Campana, 1999 ; Cadrin et al., 2013 ; Madigan et al., 2014 ; Correia et al., 2021 ; Martino et al., 2021 ; Livernois et al., 2021 ; Rooker et al., 2019 ; Rooker et al., 2021 ), as fish grows, these chemical “ signatures ” are naturally incorporated into the mineral matrix of these hard structures from ambient water and/or diet (e.g., Clarke et al., 2007 ; Elsdon et al., 2008 ; Limburg et al., 2010; Gillanders and Munro, 2012 ; Tzadik et al., 2015 ; Fowler et al., 2017; Izzo et al., 2018 ; Avigliano et al., 2019 , 2020 ).…”

“…The concentration of different chemical markers in these structures can therefore be used to discriminate among fish that spawned in or inhabited different environments and/or have distinct life histories (e.g., Smith and Whitledge, 2010 ; Sturrock et al., 2012 ; Pracheil et al., 2014 ; Starrs et al., 2016 ; Willmes et al., 2016 ; Livernois et al., 2021 ). However, the elemental composition of biomineralized structures is a function of more than just environmental conditions: physiological regulation of internal elemental composition may lead to active discrimination or preferential uptake of certain elements.…”

Inferring habitat use of the Pacific White Shark using vertebral chemistry

“…Trace elements deposited in mineralized vertebral cartilage provide additional life history information as environmental tracers (McMillan et al, 2017;Livernois et al, 2021). Controlled laboratory experiments with model elasmobranch species have demonstrated that temperature and dissolved water chemistry affect uptake of barium (Ba:Ca) in round stingrays Urobatis halleri (Smith et al, 2013) and temperature influences manganese (Mn:Ca), strontium (Sr:Ca), and Ba:Ca uptake in Port Jackson sharks (Heterodontus portusjacksoni) (Pistevos et al, 2019).…”