Bulk and amino acid nitrogen isotopes suggest shifting nitrogen balance of pregnant sharks across gestation

Shipley, Oliver N.; Olin, Jill A.; Whiteman, John P.; Bethea, Dana M.; Newsome, Seth D.

doi:10.1007/s00442-022-05197-6

Cited by 14 publications

(8 citation statements)

References 90 publications

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“…Similarly, the nitrogen physiology of deep-water sharks is unique relative to other vertebrates, whereby individuals must balance concentrations of urea and trimethylamine n -oxide to maintain osmotic balance under high hydrostatic pressures [76]. If this requires alteration to overall nitrogen balance [77], such as the mobilization of nitrogen from structural tissues to synthesize urea and/or TMAO, this may leave the residual δ 15 N values of tissues 15 N-enriched. While the δ 15 N patterns of deep-sea elasmobranchs may be linked to both physiological and ecological processes [48], low δ 13 C values for species such as Atlantic sixgill and sharpnose sevengill sharks indicate an exclusive reliance upon oceanic resource pools, suggesting these species are unlikely to be critical connectors of ecosystems.…”

Section: Discussionmentioning

confidence: 99%

Energetic connectivity of diverse elasmobranch populations – implications for ecological resilience

Shipley¹,

Matich

Hussey

et al. 2023

Proc. R. Soc. B.

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Understanding the factors shaping patterns of ecological resilience is critical for mitigating the loss of global biodiversity. Throughout aquatic environments, highly mobile predators are thought to serve as important vectors of energy between ecosystems thereby promoting stability and resilience. However, the role these predators play in connecting food webs and promoting energy flow remains poorly understood in most contexts. Using carbon and nitrogen isotopes, we quantified the use of several prey resource pools (small oceanic forage, large oceanics, coral reef, and seagrass) by 17 species of elasmobranch fishes ( n = 351 individuals) in The Bahamas to determine their functional diversity and roles as ecosystem links. We observed remarkable functional diversity across species and identified four major groups responsible for connecting discrete regions of the seascape. Elasmobranchs were responsible for promoting energetic connectivity between neritic, oceanic and deep-sea ecosystems. Our findings illustrate how mobile predators promote ecosystem connectivity, underscoring their functional significance and role in supporting ecological resilience. More broadly, strong predator conservation efforts in developing island nations, such as The Bahamas, are likely to yield ecological benefits that enhance the resilience of marine ecosystems to combat imminent threats such as habitat degradation and climate change.

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Section: Discussionmentioning

confidence: 99%

Energetic connectivity of diverse elasmobranch populations – implications for ecological resilience

Shipley¹,

Matich

Hussey

et al. 2023

Proc. R. Soc. B.

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“…Although our review focused on the main mechanisms that structure TDF variation in vertebrates, there are other factors such as physiological condition, metabolic rate, sex, ambient temperature and caloric intake that can also influence TDFs (particularly Δ 15 N; e.g. Canseco et al, 2021; Gaye‐Siessegger et al, 2004; Shipley et al, 2022). The relative effect of these variables is likely dependent on the vertebrate group, and even species, but could be used to further refine TDF estimates at the individual or population level.…”

Section: Discussionmentioning

confidence: 99%

“…TDFs are critical for accurately determining trophic position and dietary mixing scenarios (Bond & Diamond, 2011; Kjeldgaard et al, 2021; Quezada‐Romegialli et al, 2018) and are therefore foundational to attaining unbiased and robust ecological inferences. However, selecting appropriate TDFs requires careful attention, as values can differ by tissue type, trophic level and heterogeneity in diet composition (isotopic and macronutrient) (Florin et al, 2011; Hussey et al, 2014; Stephens et al, 2022) and may be further modulated by a variety of other factors including species, physiological condition, age, sex, temperature and caloric intake (Britton & Busst, 2018; Canseco et al, 2021; Gaye‐Siessegger et al, 2004; Hobson & Quirk, 2014; Kurle et al, 2014; Shipley et al, 2022).…”

Section: Introductionmentioning

confidence: 99%

Meta‐analysis and critical review of trophic discrimination factors (Δ¹³C and Δ¹⁵N): Importance of tissue, trophic level and diet source

2023

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Robustly quantifying dietary resource use and trophic position using stable isotopes requires accurate trophic discrimination factors (TDF; Δ13C and Δ15N for carbon and nitrogen, respectively), defined as the isotopic difference between consumer and diet. Early TDF studies converged on values of around 1.0‰ for Δ13C and 3.4‰ for Δ15N but more recent work indicates that TDF values may be more nuanced, depending on taxa, tissues, trophic level and diets. Yet, the relative importance of these factors remains unclear. Focusing on vertebrates (birds, fish, herptiles and mammals), we conducted a literature review of 279 studies that estimated TDF values and used a Bayesian framework to determine how tissue type, trophic level and diet source influence variation in Δ13C and Δ15N. Additionally, we reviewed 358 trophic ecology studies to determine if studies accounted for these factors during their TDF selection process. For Δ13C, vertebrates showed consistent patterns among tissue types (likely influenced by amino acid composition) and between trophic levels and diet sources (likely a result of dietary protein content and metabolic routing). Comparatively, for Δ15N, vertebrates showed considerable variation among tissue types and trophic levels, likely due to differences in tissue synthesis and physiological capabilities. Overall, Δ13C ranged from −5.1‰ to 9.1‰ and Δ15N from −3.3‰ to 9.7‰, underscoring that 1.0‰ for Δ13C and 3.4‰ for Δ15N are not universally appropriate. Moreover, both Δ13C and Δ15N varied by more than 9‰ within a single species and tissue type, demonstrating that using TDF values from the same, or similar, species may not be appropriate if diet and trophic level are not considered. Despite the importance of diet source on TDF values, most trophic ecology studies did not account for it. Further, most fish studies relied on literature review values that failed to account for tissue type, trophic level and diet source. To aid ecologists in diet and trophic assessments of vertebrates, we used our meta‐analysis to model taxon‐specific TDF estimates (mean ± SD) for each tissue type, trophic level and diet source combination. These more refined TDF values should improve ecological assessments that use stable isotopes. Read the free Plain Language Summary for this article on the Journal blog.

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“…We used the δ 15 N values of Phe to discern the δ 15 N baseline of the lake system for three reasons: (1) Phe is the most commonly employed source AA in the AA‐SIA literature, (2) Phe δ 15 N values of lake trout liver are more consistent across seasons than Lys δ 15 N values, and (3) the algal, bacterial and terrestrial energy channels supporting this lake food web are unlikely to have upregulated Phe catabolic pathways that will increase variability in baseline Phe δ 15 N values (Besser et al, 2022; Kendall et al, 2019, Ramirez et al, 2021). Offsets were calculated using several non‐essential trophic AAs (Glx and Pro) in addition to several essential trophic AAs, given that the former (e.g., Pro) may be sensitive to physiological condition (Shipley, Olin, et al, 2022; Whiteman et al, 2021) as well as diet (McMahon & McCarthy, 2016). We did not calculate absolute TP (e.g., Chikaraishi et al, 2010; Nielsen et al, 2015), given that we did not calculate β values (Δ 15 N trophic–source for primary producers) for this specific system and recent studies have found considerable variability of β values (Besser et al, 2022; Ramirez et al, 2021).…”

Section: Methodsmentioning

confidence: 99%

Energy channelling, food chain length and body condition in a northern lake predator

Shipley,

McMeans,

Besser

et al. 2023

Freshwater Biology

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Identifying potential links between food web structure and animal body condition is fundamental for predicting the long‐term persistence of populations under rapidly changing environments. Northern lakes, and the cold‐water adapted species that inhabit them, are particularly vulnerable to a warming climate. We explored relationships among body condition and energy channel use in lake trout (Salvelinus namaycush) and seasonal variation in food‐chain length in the Lake of Two Rivers, Ontario, Canada. Bayesian mixing models using carbon isotope values (δ13C) of essential amino acids showed that individuals utilising multiple energy channels had higher gonad mass, suggesting that dietary diversity has reproductive fitness benefits. Amino acid nitrogen isotope (δ15N) analysis revealed seasonal variation in food chain length, with extension of the food web during winter and spring and truncation of the food web during summer. Although these findings illustrate increased omnivory of lake trout during summer, there was no clear evidence that seasonal changes in food chain length had an impact on trout condition. These findings provide new insight into potential relationships between food web structure, energy flow and consumer condition in freshwater ecosystems, thereby revealing potential responses of species to shifting ecosystem states under intensifying climate change at high latitudes.

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Bulk and amino acid nitrogen isotopes suggest shifting nitrogen balance of pregnant sharks across gestation

Cited by 14 publications

References 90 publications

Energetic connectivity of diverse elasmobranch populations – implications for ecological resilience

Energetic connectivity of diverse elasmobranch populations – implications for ecological resilience

Meta‐analysis and critical review of trophic discrimination factors (Δ¹³C and Δ¹⁵N): Importance of tissue, trophic level and diet source

Energy channelling, food chain length and body condition in a northern lake predator

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Bulk and amino acid nitrogen isotopes suggest shifting nitrogen balance of pregnant sharks across gestation

Cited by 14 publications

References 90 publications

Energetic connectivity of diverse elasmobranch populations – implications for ecological resilience

Energetic connectivity of diverse elasmobranch populations – implications for ecological resilience

Meta‐analysis and critical review of trophic discrimination factors (Δ13C and Δ15N): Importance of tissue, trophic level and diet source

Energy channelling, food chain length and body condition in a northern lake predator

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Meta‐analysis and critical review of trophic discrimination factors (Δ¹³C and Δ¹⁵N): Importance of tissue, trophic level and diet source