Mating behavior of the lemon shark, Negaprion brevirostris (Carcharhiniformes: Carcharhinidae), as revealed by citizen science in the Equatorial Atlantic Ocean / Comportamiento de apareamiento del tiburón limón Negaprion brevirostris (Carcharhiniformes: Carcharhinidae), revelado por la ciencia ciudadana en el Océano Atlántico Ecuatorial

Introduction: Knowledge on the mating behavior and habitat requirements of large sharks, including the lemon shark, Negaprion brevirostris, is scarce, hampering conservation efforts. Objective: To describe an area in the Equatorial Atlantic used as a mating ground by N. brevirostris, as well as part of the species pre-copulatory behaviors based on citizen reports. Methods: Between 2004 and 2019, recreational divers, dive guides and rangers from the Marine Protected Area (MPA) in Fernando de Noronha Archipelago (FEN) recorded courtship behaviour, females with mating scars, pregnant females, and adult males. Results: N. brevirostris was recorded mating in shallow waters (0.5-2 m deep) during the austral summer (December to March). A specific location in the MPA, Buraco da Raquel lagoon, was the main aggregation and mating site for adult N. brevirostris in FEN. Conclusions: Citizen science records allowed the identification of shallow waters as key sites for the reproduction of this shark in FEN. Results highlight the potential of citizen science contributions to knowledge of sharks in nature and show MPAs as essential for habitat conservation of sharks with decreasing populations along the Brazilian coast, such as N. brevirostris. We present management recommendations to protect N. brevirostris there and elsewhere.

Introducción: El conocimiento sobre el comportamiento reproductivo y requisitos de hábitat de apareamiento de los tiburones grandes, incluido el tiburón limón, Negaprion brevirostris, es escaso, lo que dificulta los esfuerzos de conservación. Objetivo: Describir un área en el Océano Atlántico ecuatorial utilizada como zona de apareamiento y las interacciones precopulatorias del tiburón limón con base en informes proporcionados por ciencia ciudadana. Métodos: Buzos recreativos, guías de buceo y guardaparques del Área Marina Protegida (AMP) en el archipiélago Fernando de Noronha (FEN) llevaron registros de comportamientos de cortejo, hembras con cicatrices de apareamiento, hembras preñadas y machos adultos, entre 2004 y 2019. Resultados: Las aguas poco profundas entre 0.5 y 2 m de profundidad son utilizadas como áreas de apareamiento por N. brevirostris durante el verano austral (diciembre a marzo). Un lugar específico, dentro del AMP (laguna de Buraco da Raquel), fue identificado como el principal sitio de agregación y apareamiento de adultos de N. brevirostris en FEN. Conclusiones: Registros de ciencia ciudadana permitieron identificar aguas poco profundas como sitios clave para la reproducción de este tiburón en FEN. Los resultados resaltan el potencial de las contribuciones de la ciencia ciudadana al conocimiento de los tiburones en la naturaleza y muestran que las AMP son esenciales para la conservación del hábitat de tiburones con poblaciones decrecientes a lo largo de la costa brasileña, como N. brevirostris. Presentamos recomendaciones de gestión para proteger a N. Brevirostri, allí y en otros lugares.

Accounting for body mass effects in the estimation of field metabolic rates from body acceleration.

Dynamic body acceleration (DBA), measured through animal-attached tags, has emerged as a powerful method for estimating field metabolic rates of free-ranging individuals. Following respirometry to calibrate oxygen consumption rate (MO2) with DBA under controlled conditions, predictive models can be applied to DBA data collected from free-ranging individuals. However, laboratory calibrations are generally performed on a relatively narrow size range of animals, which may introduce biases if predictive models are applied to differently sized individuals in the field. Here, we tested the mass dependence of the MO2-DBA relationship to develop an experimental framework for the estimation of field metabolic rates when organisms differ in size. We performed respirometry experiments with individuals spanning one order of magnitude in body mass (1.74-17.15 kg) and used a two-stage modelling process to assess the intraspecific scale dependence of the MO2-DBA relationship and incorporate such dependencies into the coefficients of MO2 predictive models. The final predictive model showed scale dependence; the slope of the MO2-DBA relationship was strongly allometric (M1.55), whereas the intercept term scaled closer to isometry (M1.08). Using bootstrapping and simulations, we evaluated the performance of this coefficient-corrected model against commonly used methods of accounting for mass effects on the MO2-DBA relationship and found the lowest error and bias in the coefficient-corrected approach. The strong scale dependence of the MO2-DBA relationship indicates that caution must be exercised when models developed using one size class are applied to individuals of different sizes.

Influence of supraphysiological cortisol manipulation on predator avoidance behaviors and physiological responses to a predation threat in a wild marine teleost fish.

The stress axis in teleost fish attempts to maintain internal homeostasis in the face of allostatic loading. However, stress axis induction has been associated with a higher predation rate in fish. To date, the physiological and behavioral factors associated with this outcome are poorly understood. The purpose of the present study was to investigate the impact of experimental cortisol elevation on anti-predator behavior and physiological responses to predator presence. We hypothesized that semi-chronic cortisol elevation would increase susceptibility to predation by increasing stress-induced risk-taking behaviors. To test this hypothesis, schoolmaster snapper were given cocoa butter implants without cortisol (sham) or with cortisol (50 mg/kg body weight) and tethered to cover. Fish were exposed to either a lemon shark or control conditions for 15-min. Space use and activity were recorded throughout and fish were terminally sampled for blood. Cortisol implantation, relative to shams, resulted in higher blood glucose and plasma cortisol concentrations with a lower plasma lactate concentration. Shark exposure, relative to controls, elicited higher blood glucose and lactate concentrations but had no effect on plasma cortisol concentration. No interactions were detected between shark exposure and cortisol treatment for any physiological trait. Behavioral metrics, including shelter use and activity, were unaffected by either cortisol implantation or shark exposure. Physiological responses to cortisol implantation likely resulted from enhanced gluconeogenic activity, whereas alterations under predator exposure may have been the product of catecholamine mobilization. Further work should address context-specific influences of stress in mediating behavioral responses to predation.

Risky business for a juvenile marine predator? Testing the influence of foraging strategies on size and growth rate under natural conditions.

Mechanisms driving selection of body size and growth rate in wild marine vertebrates are poorly understood, thus limiting knowledge of their fitness costs at ecological, physiological and genetic scales. Here, we indirectly tested whether selection for size-related traits of juvenile sharks that inhabit a nursery hosting two dichotomous habitats, protected mangroves (low predation risk) and exposed seagrass beds (high predation risk), is influenced by their foraging behaviour. Juvenile sharks displayed a continuum of foraging strategies between mangrove and seagrass areas, with some individuals preferentially feeding in one habitat over another. Foraging habitat was correlated with growth rate, whereby slower growing, smaller individuals fed predominantly in sheltered mangroves, whereas larger, faster growing animals fed over exposed seagrass. Concomitantly, tracked juveniles undertook variable movement behaviours across both the low and high predation risk habitat. These data provide supporting evidence for the hypothesis that directional selection favouring smaller size and slower growth rate, both heritable traits in this shark population, may be driven by variability in foraging behaviour and predation risk. Such evolutionary pathways may be critical to adaptation within predator-driven marine ecosystems.

Three decades of longlining in Bimini, Bahamas, reveals long-term trends in lemon shark Negaprion brevirostris (Carcharhinidae) catch per unit effort.

In Bimini, Bahamas, the consistent employment of longlines, beginning in 1982, provided a rare opportunity to explore population trends for large resident sharks. This study assessed three shallow water longline survey periods at this location; 1982-1989, 1992-2002 and 2003-2014, with the aim of determining trends in annual catch per unit effort (CPUE) for an IUCN listed near-threatened species, the lemon shark Negaprion brevirostris. A general additive model (GAM) was used to analyse the non-linear annual CPUE values over the entire 32-year research period. The GAM displayed high variability of annual CPUE, with a peak value of 0·026 N. brevirostris per hook day (hooks day(-1) ) in 2000. The temporal pattern of CPUE indicated an abundance trend with a complete cycle, from trough to trough, occurring over a period of approximately 18 years. The 1982-1989 survey period saw the highest proportion of mature individuals (19·8%) and the smallest average pre-caudal length (LPC ; 124·8 cm). The 1992-2002 survey period had the highest average annual CPUE (0·018 hooks day(-1) ), while the 2003-2014 research period saw largest average LPC size (134·8 cm) and the lowest average CPUE values (0·009 hooks day(-1) ) of the entire research period. The long-term trend identified in this study provides a baseline for future assessment.

Bioaccumulation of organohalogenated compounds in sharks and rays from the southeastern USA.

Organohalogenated compounds are widespread in the marine environment and can be a serious threat to organisms in all levels of aquatic food webs, including elasmobranch species. Information about the concentrations of POPs (persistent organic pollutants) and of MeO-PBDEs (methoxylated polybrominated diphenyl ethers) in elasmobranchs is scarce and potential toxic effects are poorly understood. The aims of the present study were therefore to investigate the occurrence of multiple POP classes (PCBs, PBDEs, DDXs, HCB, CHLs) and of MeO-PBDEs in various elasmobranch species from different trophic levels in estuarine and marine waters of the southeastern United States. Overall, levels and patterns of PCBs, PBDEs, DDXs, HCB, CHLs and of MeO-PBDEs varied according to the species, maturity stage, gender and habitat type. The lowest levels of POPs were found in Atlantic stingrays and the highest levels were found in bull sharks. As both species are respectively near the bottom and at top of the trophic web, with juvenile bull sharks frequently feeding on Atlantic stingrays, these findings further suggest a bioaccumulation and biomagnification process with trophic position. MeO-PBDEs were not detected in Atlantic stingrays, but were found in all shark species. HCB was not found in Atlantic stingrays, bonnetheads or lemon sharks, but was detected in the majority of bull sharks examined. Comparison with previous studies suggests that Atlantic stingrays may be experiencing toxic effects of PCBs and DDXs on their immune system. However, the effect of these compounds on the health of shark species remains unclear.

Hooking injury, physiological status and short-term mortality of juvenile lemon sharks (Negaprion bevirostris) following catch-and-release recreational angling.

Sport fishing for sharks, including fishing with the intent to release, is becoming more prevalent within the recreational angling community. Common targets of recreational anglers are juvenile lemon sharks (Negaprion brevirostris) that frequent shallow tropical nearshore habitats. In this study, we captured 32 juvenile lemon sharks (530-875 mm total length) with conventional angling gear (i.e. spinning rods, dead fish bait and 5/0 barbed circle hooks) from the coastal waters of Eleuthera, The Bahamas, to determine the consequences of capture for individual sharks. Each shark was examined for hooking injuries, blood sampled to quantify physiological disturbance, assessed for reflex impairment and then monitored to assess post-release behaviour and mortality. Four sharks (12.5%) died following release during the 15 min tracking period. Principal components (PC) analysis revealed four axes describing 66.5% of the variance for blood physiology parameters, total length and water temperature. The PC1 and PC3 scores, characterized by positive factor loadings for indicators of exercise-induced stress and blood ion concentrations, respectively, were significantly related to fight time but were not associated with short-term mortality. Short-term mortality was significantly related to factor scores for PC4 that loaded heavily for water temperature and total length. Ten sharks (31%) exhibited impaired reflexes, with loss of bite reflex being most prevalent. Sharks that died had the following characteristics: (i) they had two or more impaired reflexes; (ii) they were hooked in the basihyal; (iii) they exhibited no movement after the initial bout of directional swimming; and (iv) they experienced high water temperatures (i.e. >31°C). Collectively, these results indicate that for juvenile lemon sharks inhabiting tropical flats, fight time can influence the degree of physiological disturbance, while water temperature contributes to the likelihood of survival following release.