Science of the Total Environment 780 (2021) 146548 Contents lists available at ScienceDirect Science of the Total Environment journal homepage: www.elsevier.com/locate/scitotenv Metabolic and nutritional condition of juvenile tiger sharks exposed to regional differences in coastal urbanization Bianca de Sousa Rangel a,⁎, Renata Guimarães Moreira a, Yuri Vieira Niella b, James A. Sulikowski c, Neil Hammerschlag d,e a Laboratório de Metabolismo e Reprodução de Organismos Aquáticos, Departamento de Fisiologia, Instituto de Biociências, Universidade de São Paulo, Rua do Matão, travessa 14, 321, CEP 05508- 090, Cidade Universitária, São Paulo, SP, Brazil b Department of Biological Sciences, Macquarie University, North Ryde, New South Wales 2113, Australia c School of Mathematical and Natural Sciences, Arizona State University, Glendale, AZ 85306, USA d Rosenstiel School of Marine and Atmospheric Science, University of Miami, Miami, FL 33149, USA e Leonard and Jayne Abess Center for Ecosystem Science and Policy, University of Miami, Coral Gables, FL 33146, USA HIGHLIGHTS GRAPHICAL ABSTRACT • Corticosterone levels were higher in ju- venile tiger sharks sampled in Florida • Thyroid hormones did not differ in tiger sharks sampled in both regions • Tiger sharks sampled in Florida had higher proportions of omega-3 PUFA • Tiger sharks sampled in the Bahamas had higher proportions of bacterial markers • No apparent relation between location and nutritional quality or metabolic hormones. article info abstract Article history: How varying levels of human activity, such as proximity and size of the nearest market (i.e., market gravity), Received 18 January 2021 influence the nutritional ecology and physiological condition of highly migratory marine predators is poorly Received in revised form 8 March 2021 understood. In the present study, we used a non-lethal approach to compare the concentration of metabolic Accepted 13 March 2021 hormones (i.e. corticosteroids and thyroid hormones) and plasma fatty acids between juvenile female tiger Available online 18 March 2021 sharks (Galeocerdo cuvier) sampled in two areas of the subtropical north Atlantic, which differed markedly Editor: Julian Blasco in their levels of coastal urbanization, Florida and the Bahamas (high versus low, respectively). We hypoth- esized that juvenile female tiger sharks sampled in water surrounding high coastal urbanization (Florida), would exhibit evidence of lower prey quality and higher energetic demands as compared to individuals Keywords: sampled in relatively less urbanized areas of Northern Bahamas. Results revealed that relative corticoste- Galeocerdo cuvier roid levels (a proxy for energy mobilization) were higher in juvenile female tiger sharks sampled in Florida; Urban ecology however, no differences were found in concentrations of thyroid hormones (proxies of energetic adjust- Marine predator ments) between the two locations. We found higher percentages of omega-3 polyunsaturated fatty acids Fatty acids (indicative of high prey quality) in juvenile tiger sharks from Florida, whereas higher percentages of bacte- Corticosteroids rial markers (often indicative of domestic sewage effluent) were detected in the individuals sampled in the Thyroid hormones fi Nutritional ecology Bahamas. Taken together, these ndings do not suggest that the differences in nutritional quality and met- Market gravity abolic condition found between the two sampling locations can be fully attributed to foraging in areas ⁎ Corresponding author. E-mail address: [email protected] (B.S. Rangel). https://doi.org/10.1016/j.scitotenv.2021.146548 0048-9697/© 2021 Elsevier B.V. All rights reserved. B.S. Rangel, R.G. Moreira, Y.V. Niella et al. Science of the Total Environment 780 (2021) 146548 exposed to differing levels of urbanization. We speculate that these patterns may be due to the highly mi- gratory nature and generalist feeding strategy of this species, even at the juvenile life stage, as well as prox- imity of sampling locations from shore. ©2021ElsevierB.V.Allrightsreserved. 1. Introduction nutritional quality compared to tiger sharks sampled in relatively more pristine waters (the northern Bahamas, Fig. 1). Assessing the nutritional ecology of predators at relevant spatial To test this hypothesis, we compared metabolic hormones (i.e. scales is critical for understanding patterns of habitat use and their in- relative corticosteroids and thyroid hormones) and fatty acid dietary fluence on food web structure and nutrient cycling (e.g. Estes et al., markers in juvenile tiger sharks sampled in South Florida and the north- 2016; Hammerschlag et al., 2019). For instance, regional variation in di- ern Bahamas. The relative corticosteroid concentrations were used as a etary patterns of predators can be driven by ontogenetic variations proxy for energy mobilization. Glucocorticoid concentrations fluctuate (Aines et al., 2018; Dicken et al., 2017), food availability, prey prefer- according to energetic demands, increasing in response to anticipated ences (Acuña-Marrero et al., 2017; Salinas-de-León et al., 2019), intra- or perceived environmental changes (Romero, 2002; McEwen and and interspecific interactions (Every et al., 2019), as well as by urbaniza- Wingfield, 2003), for example increasing during long-term food depri- tion (Rangel et al., 2021a) and tourism provisioning (Semeniuk et al., vation (e.g. Lynn et al., 2003; Iki et al., 2020). The thyroid hormones 2009; Meyer et al., 2019). Such knowledge is particularly relevant for (thyroxine [T4] and triiodothyronine [T3]) are important mediators in highly migratory predators, such as large sharks, due to their wide the regulation of development and metabolic rate in vertebrates, and areas of space use and high energetic requirements (e.g. Estes et al., therefore, are attractive biomarkers to investigate energetic adjust- 2016; Hammerschlag et al., 2019). ments (e.g. Norris and Carr, 2013; Behringer et al., 2018). Based on The tiger shark (Galeocerdo cuvier)isalarge-bodiedgeneralist our hypothesis, we expected that juvenile tiger sharks occupying predator (growing up to 5.5 m in length), which exhibits consider- water adjacent to high levels of coastal urbanization would exhibit able variability in habitat use and movements patterns, making this higher concentrations of these metabolic hormones, compared to indi- species an interesting model for investigating the effects of spatial viduals sampled in waters adjacent to low levels of coastal urbanization. variation on marine predator nutritional ecology (Hammerschlag Plasma fatty acid profiles were used as short-term dietary markers to et al., 2012; Papastamatiou et al., 2013; Lea et al., 2015, 2018; make inferences about prey quality (McMeans et al., 2012; Beckmann Ajemian et al., 2020). Tiger sharks exploit a wide variety of prey, in- et al., 2014; Rangel et al., 2020, 2021a), and basal food chain dependencies cluding invertebrates, teleosts, elasmobranchs, reptiles, seabirds and (e.g., bacteria, diatoms, dinoflagellates; Dalsgaard et al., 2003). Because marine mammals, with prey diversity and size expanding with on- fatty acids are transferred with little modification from prey to predator, togeny (e.g. Aines et al., 2018; Dicken et al., 2017). Recent studies they are especially relevant biomarkers to study diet patterns and nutri- showed that despite being an opportunistic forager, their dietary pat- tional shifts in the urbanization context (Budge et al., 2006; Iverson, terns, nutritional and metabolic condition are life stage-dependent, sug- 2009; Gomes et al., 2016). Moreover, consumers are unable to produce gesting female tiger shark can adjust their nutritional and metabolic de novo omega-3 and -6 polyunsaturated fatty acids (n3 and n6 PUFAs) requirement during reproduction (Hammerschlag et al., 2018; Rangel and limited in their ability in converting them to highly unsaturated et al., 2021b). fatty acids. Therefore, the consumers rely on the diet to obtain PUFAs, At younger life stages, tiger sharks tend to occupy and forage more in such as docosahexaenoic acid (DHA, C22:6n3), arachidonic acid (ARA, coastal inshore waters, expanding their range to offshore waters as C20:4n6) and eicosapentaenoic acid (EPA, C20:5n3) (Dalsgaard et al., adults (e.g. Lea et al., 2018; Ajemian et al., 2020). While nearshore wa- 2003; Budge et al., 2006). Because these PUFAs have crucial functions in ters can offer abundant food and provide shelter from predators (e.g. a variety of physiological processes, an inadequate dietary intake of Heupel et al., 2007), juvenile sharks using these environments are ex- PUFAs can compromise the individual's health and survival (Izquierdo posed to numerous anthropogenic disturbances associated with coastal et al., 2001; Tocher, 2010; Birnie-Gauvin et al., 2017). Based on our development and urban sprawl, including habitat loss, fishing and pol- hypothesis, we predicted that juvenile tiger sharks exposed to greater lution (Knip et al., 2010). Moreover, primary productivity is often dra- market gravity would have higher proportions of saturated (SFA) and matically modified in inshore areas exposed to such urbanization, thus bacterial fatty acids, as these biomarkers are often highly correlated altering food availability and quality for marine predators through bot- with domestic sewage effluent (e.g. Boëchat et al., 2014; Jiménez- tom up processes (Faeth et al., 2005; El-Sabaawi, 2018). Indeed, numer- Martínez et al., 2019). We also anticipated that juvenile tiger sharks sam-