First report on the serum chemistry and haematology of free-ranging dusky (Carcharhinus obscurus) and sandbar (Carcharhinus plumbeus) sharks in the eastern Mediterranean Sea

Abstract

Shark assessments in the Mediterranean Sea are still scarce, and serum chemistry and haematological data have yet to be reported for wild dusky (Carcharhinus obscurus) or sandbar (Carcharhinus plumbeus) shark populations in the Mediterranean Sea. Herein, blood samples were obtained from adult dusky (n = 23) and sandbar (n = 14) sharks from an aggregation site near the Hadera power and desalination plants in Israel in the winters of 2016–20. Several serum chemistry analytes were characterized with relation to stress, body size and environmental conditions. Glucose concentrations were higher, while total cholesterol concentrations were lower in dusky sharks than in sandbar sharks, potentially due to distinct metabolic pathways utilized during the capture-related activity by both species. However, differences in sex and size are noted and should be considered. The blood cell morphology of both species was consistent with previous findings for sandbar sharks. Atypical monocytes were noted in one dusky shark. Preliminary and exploratory reference intervals for female dusky sharks were calculated for glucose, triglycerides, total cholesterol, total protein and creatine kinase. These data must be viewed with caution due to the potential influence of capture-related stress on analyte concentrations and activities and the fact that only females were employed in the calculations. Moreover, the sampling site is adjacent to coastal power and desalination plants, which may significantly affect shark physiology. Although limited, this novel database on dusky and sandbar shark serum chemistry and haematology aspects is essential as a first attempt to obtain data on these species in the eastern Mediterranean Sea and for future conservation and long-term biomonitoring efforts.

Serum chemistry, thyroxine concentration, and blood cell morphology of wild, young Blackchin Guitarfish Glaucostegus cemiculus sampled on the eastern Mediterranean coastline

“…Typical thrombocyte morphology in elasmobranchs closely resembles that in nonmammalian species (Haines and Arnold 2014;Arnold and Delaune 2022). The thrombocytes of Blackchin Guitarfish were morphologically very similar to those generally described in elasmobranchs (Ellis 1977;Arnold 2005;Arnold and Delaune 2022;Starostinetsky-Malonek et al 2023). In certain elasmobranchs (e.g., skates and rays; Haines and Arnold 2014) but not in Blackchin Guitarfish, a second thrombocyte population (also termed "G4 cells") was described, with a shape very similar to that of typical thrombocytes but differing in the presence of many slender, rod-shaped cytoplasmic eosinophilic (azurophilic) granules; their function and clinical significance are yet unclear (Hyder et al 1983;Arnold 2005;Haines and Arnold 2014;Arnold and Delaune 2022).…”

“…Neutrophils were described in a minority of elasmobranch species, mostly with somewhat different morphology than that noted herein (Haines and Arnold 2014). Neutrophils were described in the Sandbar Shark (Arnold 2005;Starostinetsky-Malonek et al 2023), the Spotted Eagle Ray Aetobatus narinari (Arnold and Delaune 2022), and at least three different rhinobatid species (i.e., Common Guitarfish, Eastern Fiddler Ray Trygonorrhina fasciata, and Thornback Guitarfish Platyrhinoidis triseriata; Haines and Arnold 2014) as well as other rhinobatids (Stacy et al 2022). Neutrophil function in sharks was demonstrated to include phagocytosis (e.g., antibody-mediated phagocytosis) and enzyme-based killing mechanisms (Haines and Arnold 2014), although their ultrastructure differs from that of teleost or mammalian neutrophils.…”

“…Leukocytes that were presumed to be immature neutrophils (diameter = 11-13 μm), resembling the neutrophils described in the Sandbar Shark Carcharhinus plumbeus (Arnold 2005;Starostinetsky-Malonek et al 2023) and in Blackchin Guitarfish (Carmezim and Marcos 2020), were noted in six individuals (14%), being rare in some and commonly observed in others (Figure 8). They contained numerous, very weakly and neutrally stained (sometimes unstained) cytoplasmic granules.…”

Serum chemistry, thyroxine concentration, and blood cell morphology of wild, young Blackchin Guitarfish Glaucostegus cemiculus sampled on the eastern Mediterranean coastline

“…Typical thrombocyte morphology in elasmobranchs closely resembles that in nonmammalian species (Haines and Arnold 2014;Arnold and Delaune 2022). The thrombocytes of Blackchin Guitarfish were morphologically very similar to those generally described in elasmobranchs (Ellis 1977;Arnold 2005;Arnold and Delaune 2022;Starostinetsky-Malonek et al 2023). In certain elasmobranchs (e.g., skates and rays; Haines and Arnold 2014) but not in Blackchin Guitarfish, a second thrombocyte population (also termed "G4 cells") was described, with a shape very similar to that of typical thrombocytes but differing in the presence of many slender, rod-shaped cytoplasmic eosinophilic (azurophilic) granules; their function and clinical significance are yet unclear (Hyder et al 1983;Arnold 2005;Haines and Arnold 2014;Arnold and Delaune 2022).…”

“…Neutrophils were described in a minority of elasmobranch species, mostly with somewhat different morphology than that noted herein (Haines and Arnold 2014). Neutrophils were described in the Sandbar Shark (Arnold 2005;Starostinetsky-Malonek et al 2023), the Spotted Eagle Ray Aetobatus narinari (Arnold and Delaune 2022), and at least three different rhinobatid species (i.e., Common Guitarfish, Eastern Fiddler Ray Trygonorrhina fasciata, and Thornback Guitarfish Platyrhinoidis triseriata; Haines and Arnold 2014) as well as other rhinobatids (Stacy et al 2022). Neutrophil function in sharks was demonstrated to include phagocytosis (e.g., antibody-mediated phagocytosis) and enzyme-based killing mechanisms (Haines and Arnold 2014), although their ultrastructure differs from that of teleost or mammalian neutrophils.…”

“…Leukocytes that were presumed to be immature neutrophils (diameter = 11-13 μm), resembling the neutrophils described in the Sandbar Shark Carcharhinus plumbeus (Arnold 2005;Starostinetsky-Malonek et al 2023) and in Blackchin Guitarfish (Carmezim and Marcos 2020), were noted in six individuals (14%), being rare in some and commonly observed in others (Figure 8). They contained numerous, very weakly and neutrally stained (sometimes unstained) cytoplasmic granules.…”

Standardized protocols for blood collection and analysis in elasmobranchs: a practical guide for clinicians and researchers

“…The step-by-step procedures outlined for venipuncture, blood gas analysis, hematology, biochemistry, and plasma protein electrophoresis are designed to be implementable with common veterinary equipment, thereby maximizing their practical utility. A key advantage of this harmonized approach is its potential to support the development of robust, longitudinal databases, which are indispensable for establishing statistically valid, species-specific reference intervals, a foundational element currently lacking in elasmobranch medicine ( 22 ). For instance, the consistent use of modified Natt-Herrick’s solution and the formalin-based preservation technique for delayed cell counts address specific analytical pitfalls related to elasmobranch blood osmolarity and sample stability ( 2 , 37 ).…”

Unveiling the biochemical and haematological profile of blue shark (Prionace glauca) in the Mediterranean after bycatch

“…, 2012 ), including shark species from the same geographic zone ( Falco et al. , 2023 ; Starostinetsky-Malonek et al. , 2023 ), although inter-species variability can be observed, and other blue shark populations from other geographic areas ( Hight et al.…”

Serum chemistry, thyroxine concentration, and blood cell morphology of wild, young Blackchin Guitarfish Glaucostegus cemiculus sampled on the eastern Mediterranean coastline

“…Typical thrombocyte morphology in elasmobranchs closely resembles that in nonmammalian species (Haines and Arnold 2014;Arnold and Delaune 2022). The thrombocytes of Blackchin Guitarfish were morphologically very similar to those generally described in elasmobranchs (Ellis 1977;Arnold 2005;Arnold and Delaune 2022;Starostinetsky-Malonek et al 2023). In certain elasmobranchs (e.g., skates and rays; Haines and Arnold 2014) but not in Blackchin Guitarfish, a second thrombocyte population (also termed "G4 cells") was described, with a shape very similar to that of typical thrombocytes but differing in the presence of many slender, rod-shaped cytoplasmic eosinophilic (azurophilic) granules; their function and clinical significance are yet unclear (Hyder et al 1983;Arnold 2005;Haines and Arnold 2014;Arnold and Delaune 2022).…”

“…Neutrophils were described in a minority of elasmobranch species, mostly with somewhat different morphology than that noted herein (Haines and Arnold 2014). Neutrophils were described in the Sandbar Shark (Arnold 2005;Starostinetsky-Malonek et al 2023), the Spotted Eagle Ray Aetobatus narinari (Arnold and Delaune 2022), and at least three different rhinobatid species (i.e., Common Guitarfish, Eastern Fiddler Ray Trygonorrhina fasciata, and Thornback Guitarfish Platyrhinoidis triseriata; Haines and Arnold 2014) as well as other rhinobatids (Stacy et al 2022). Neutrophil function in sharks was demonstrated to include phagocytosis (e.g., antibody-mediated phagocytosis) and enzyme-based killing mechanisms (Haines and Arnold 2014), although their ultrastructure differs from that of teleost or mammalian neutrophils.…”

“…Leukocytes that were presumed to be immature neutrophils (diameter = 11-13 μm), resembling the neutrophils described in the Sandbar Shark Carcharhinus plumbeus (Arnold 2005;Starostinetsky-Malonek et al 2023) and in Blackchin Guitarfish (Carmezim and Marcos 2020), were noted in six individuals (14%), being rare in some and commonly observed in others (Figure 8). They contained numerous, very weakly and neutrally stained (sometimes unstained) cytoplasmic granules.…”

Standardized protocols for blood collection and analysis in elasmobranchs: a practical guide for clinicians and researchers

“…The step-by-step procedures outlined for venipuncture, blood gas analysis, hematology, biochemistry, and plasma protein electrophoresis are designed to be implementable with common veterinary equipment, thereby maximizing their practical utility. A key advantage of this harmonized approach is its potential to support the development of robust, longitudinal databases, which are indispensable for establishing statistically valid, species-specific reference intervals, a foundational element currently lacking in elasmobranch medicine ( 22 ). For instance, the consistent use of modified Natt-Herrick’s solution and the formalin-based preservation technique for delayed cell counts address specific analytical pitfalls related to elasmobranch blood osmolarity and sample stability ( 2 , 37 ).…”

Unveiling the biochemical and haematological profile of blue shark (Prionace glauca) in the Mediterranean after bycatch

“…, 2012 ), including shark species from the same geographic zone ( Falco et al. , 2023 ; Starostinetsky-Malonek et al. , 2023 ), although inter-species variability can be observed, and other blue shark populations from other geographic areas ( Hight et al.…”

Serum chemistry, thyroxine concentration, and blood cell morphology of wild, young Blackchin Guitarfish Glaucostegus cemiculus sampled on the eastern Mediterranean coastline

“…Typical thrombocyte morphology in elasmobranchs closely resembles that in nonmammalian species (Haines and Arnold 2014;Arnold and Delaune 2022). The thrombocytes of Blackchin Guitarfish were morphologically very similar to those generally described in elasmobranchs (Ellis 1977;Arnold 2005;Arnold and Delaune 2022;Starostinetsky-Malonek et al 2023). In certain elasmobranchs (e.g., skates and rays; Haines and Arnold 2014) but not in Blackchin Guitarfish, a second thrombocyte population (also termed "G4 cells") was described, with a shape very similar to that of typical thrombocytes but differing in the presence of many slender, rod-shaped cytoplasmic eosinophilic (azurophilic) granules; their function and clinical significance are yet unclear (Hyder et al 1983;Arnold 2005;Haines and Arnold 2014;Arnold and Delaune 2022).…”

“…Neutrophils were described in a minority of elasmobranch species, mostly with somewhat different morphology than that noted herein (Haines and Arnold 2014). Neutrophils were described in the Sandbar Shark (Arnold 2005;Starostinetsky-Malonek et al 2023), the Spotted Eagle Ray Aetobatus narinari (Arnold and Delaune 2022), and at least three different rhinobatid species (i.e., Common Guitarfish, Eastern Fiddler Ray Trygonorrhina fasciata, and Thornback Guitarfish Platyrhinoidis triseriata; Haines and Arnold 2014) as well as other rhinobatids (Stacy et al 2022). Neutrophil function in sharks was demonstrated to include phagocytosis (e.g., antibody-mediated phagocytosis) and enzyme-based killing mechanisms (Haines and Arnold 2014), although their ultrastructure differs from that of teleost or mammalian neutrophils.…”

“…Leukocytes that were presumed to be immature neutrophils (diameter = 11-13 μm), resembling the neutrophils described in the Sandbar Shark Carcharhinus plumbeus (Arnold 2005;Starostinetsky-Malonek et al 2023) and in Blackchin Guitarfish (Carmezim and Marcos 2020), were noted in six individuals (14%), being rare in some and commonly observed in others (Figure 8). They contained numerous, very weakly and neutrally stained (sometimes unstained) cytoplasmic granules.…”

Standardized protocols for blood collection and analysis in elasmobranchs: a practical guide for clinicians and researchers

“…The step-by-step procedures outlined for venipuncture, blood gas analysis, hematology, biochemistry, and plasma protein electrophoresis are designed to be implementable with common veterinary equipment, thereby maximizing their practical utility. A key advantage of this harmonized approach is its potential to support the development of robust, longitudinal databases, which are indispensable for establishing statistically valid, species-specific reference intervals, a foundational element currently lacking in elasmobranch medicine ( 22 ). For instance, the consistent use of modified Natt-Herrick’s solution and the formalin-based preservation technique for delayed cell counts address specific analytical pitfalls related to elasmobranch blood osmolarity and sample stability ( 2 , 37 ).…”

Unveiling the biochemical and haematological profile of blue shark (Prionace glauca) in the Mediterranean after bycatch

“…, 2012 ), including shark species from the same geographic zone ( Falco et al. , 2023 ; Starostinetsky-Malonek et al. , 2023 ), although inter-species variability can be observed, and other blue shark populations from other geographic areas ( Hight et al.…”