Shark tooth collagen stable isotopes (δ¹⁵N and δ¹³C) as ecological proxies

Abstract

1. The isotopic composition of tooth-bound collagen has long been used to reconstruct dietary patterns of animals in extant and palaeoecological systems. For sharks that replace teeth rapidly in a conveyor-like system, stable isotopes of tooth collagen (δ 13 C Teeth & δ 15 N Teeth ) are poorly understood and lacking in ecological context relative to other non-lethally sampled tissues. This tissue holds promise, because shark jaws may preserve isotopic chronologies from which to infer individual-level ecological patterns across a range of temporal resolutions.2. Carbon and nitrogen stable isotope values were measured and compared between extracted tooth collagen and four other non-lethally sampled tissues of varying isotopic turnover rates: blood plasma, red blood cells, fin and muscle, from eight species of sharks. Individual-level isotopic variability of shark tooth collagen was evaluated by profiling teeth of different ages across whole jaws for the shortfin mako shark Isurus oxyrinchus and sandbar shark Carcharhinus plumbeus.3. Measurements of δ 13 C Teeth and δ 15 N Teeth were positively correlated with isotopic values from the four other tissues. Collagen δ 13 C was consistently 13 C-enriched relative to all other tissues. Patterns for δ 15 N were slightly less uniform; tooth collagen was generally 15 N-enriched relative to muscle and red blood cells, but congruent with fin and blood plasma (values clustered around a 1:1 relationship). 4. Significant within-individual variability was observed across whole shortfin mako shark (δ 13 C range = 1.4‰, δ 15 N range = 3.6‰) and sandbar shark (δ 13 C range = 1.2‰-2.4‰, δ 15 N range = 1.7‰-2.4‰) jaws, which trended with tooth age.5. We conclude that amino acid composition and associated patterns of isotopic fractionation result in predictable isotopic offsets between tissues. Within-individual variability of tooth collagen stable isotope values suggests teeth of different ages may serve as ecological chronologies, that could be applied to studies on migration and individuallevel diet variation across diverse time-scales. Greater understanding of tooth replacement rates, isotopic turnover and associated fractionation of tooth collagen will help refine potential ecological inferences, outlining clear goals for future scientific inquiry.

Cenozoic megatooth sharks occupied extremely high trophic positions

“…While dentin collagen is not a reliable source of organic nitrogen in ancient fossils, the δ 15 N of dentin collagen in modern sharks has been established as a trophic level proxy that robustly records variations in the dietary δ 15 N value ( 33 , 34 ). As dentin collagen and enameloid are formed over similar time frames, we expect that the δ 15 N values of these tissues should covary in response to diet and physiology.…”

“…This enameloid TDF is consistent with a recent controlled feeding experiment that estimated TDF values for rodent tooth enamel bound organic matter δ 15 N between 1.9 and 4.9‰ ( 19 ). The δ 15 N EB values of sharks can be related to δ 15 N measurements of other shark tissues (muscle, plasma, red blood cells, and fin) through their comparison to dentin collagen δ 15 N ( 33 , 34 ). Notably, dentin collagen δ 15 N is on average 1.9 ± 0.7‰ lower than muscle δ 15 N ( 34 ).…”

“…The δ 15 N EB values of sharks can be related to δ 15 N measurements of other shark tissues (muscle, plasma, red blood cells, and fin) through their comparison to dentin collagen δ 15 N ( 33 , 34 ). Notably, dentin collagen δ 15 N is on average 1.9 ± 0.7‰ lower than muscle δ 15 N ( 34 ). Combined with our observations of δ 15 N EB values that are on average 1.7 ± 0.5‰ higher than dentin collagen δ 15 N, this suggests that δ 15 N EB should closely match shark muscle δ 15 N. Future studies should sample a broader range of dentin collagen δ 15 N and δ 15 N EB to validate the offset we propose.…”

Integrating isotopic and nutritional niches reveals multiple dimensions of individual diet specialisation in a marine apex predator

“…As with other elasmobranchs, sharks develop teeth continuously below the jawline which rotate forwards in files in a conveyor belt style process to replace existing functional teeth on the outer jaw edge (Figure 2 ). Thereby, sampling tooth rows within a file from the inner (newest tooth) to outer jaw edge (oldest tooth) provides a sequential record of foraging patterns over temporally distinct periods (when each tooth formed) defined by rates of tooth replacement and isotopic turnover during odontogenesis (Shipley et al, 2021 ).…”

“…Svanback et al, 2015 ), since they only resolve WIC at interannual or greater timescales (across multiple years). Therefore, we used a novel approach, sampling sequentially formed tooth files, the potential of which for fine‐scale (month increment) individual‐level diet reconstruction in elasmobranchs has been recently highlighted (Shipley et al, 2021 ; Zeichner et al, 2017 ), analogous to more widely used systems in other species (e.g. mammalian hair/vibrissae; Newsome et al, 2009 ).…”