A global perspective on the trophic geography of sharks

Bird, Christopher S.; Veríssimo, Ana; Magozzi, Sarah; Abrantes, Kátya G.; Aguilar, Àlex; Al-Reasi, Hassan A.; Barnett, Adam; Bethea, Dana M.; Biais, Gerard; Borrell, Asunción; Bouchoucha, Marc; Boyle, Mariah; Brooks, Edward J.; Brunnschweiler, Juerg M.; Bustamante, Paco; Carlisle, Aaron B.; Catarino, Diana; Caut, Stéphane; Cherel, Yves; Chouvelon, Tiphaine; Churchill, Diana; Ciancio, Javier; Claes, Julien; Colaço, Ana; Courtney, Dean L.; Cresson, Pierre; Daly, Ryan; Necker, Leigh De; Endo, Tokiko; Figueiredo, Ivone; Frisch, Ashley J.; Hansen, Joan Holst; Heithaus, Michael R.; Hussey, Nigel E.; Iitembu, Johannes A.; Juanes, Francis; Kinney, Michael J.; Kiszka, Jérémy J.; Klarian, Sebastián A.; Kopp, Dorothée; Leaf, Robert T.; Li, Yunkai; Lorrain, Anne; Madigan, Daniel J.; Maljković, Aleksandra; Malpica-Cruz, Luis; Matich, Philip; Meekan, Mark G.; Ménard, Frédéric; Menezes, Gui; Munroe, Samantha; Newman, Michael C.; Papastamatiou, Yannis P.; Pethybridge, Heidi; Plumlee, Jeffrey D.; Polo-Silva, Carlos; Quaeck-Davies, Katie; Raoult, Vincent; Reum, Jonathan C. P.; Torres‐Rojas, Yassir Edén; Shiffman, David S.; Shipley, Oliver N.; Speed, Conrad W.; Staudinger, Michelle D.; Teffer, Amy K.; Tilley, Alexander; Valls, María; Vaudo, Jeremy J.; Wai, Tak Cheung; Wells, R. J. David; Wyatt, Alex S. J.; Yool, Andrew; Trueman, Clive N.

doi:10.1038/s41559-017-0432-z

Cited by 101 publications

(79 citation statements)

References 43 publications

(50 reference statements)

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“…Changes in tuna δ 13 C values can in turn be described by the following equation:

{normalδ}^{13} {normalC}_{tuna} = \frac{1}{()(, 1 + \frac{ε_{fc}}{1, 000})} ({normalδ}^{13} {normalC}_{normalp} - ε_{fc}),

where ε fc is the overall fractionation associated with trophic transfers and is considered to be low (~0.5‰ to 1.8‰ per trophic level), therefore we used 4‰ for tuna that are considered to be at a trophic position of ~4 (Olson et al, ). As a comparison, Bird et al () found an average difference of 4.6‰ between phytoplankton and sharks on a global scale.…”

Section: Methodsmentioning

confidence: 99%

Trends in tuna carbon isotopes suggest global changes in pelagic phytoplankton communities

Lorrain

Pethybridge

Cassar

et al. 2019

Global Change Biology

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Considerable uncertainty remains over how increasing atmospheric CO2 and anthropogenic climate changes are affecting open‐ocean marine ecosystems from phytoplankton to top predators. Biological time series data are thus urgently needed for the world's oceans. Here, we use the carbon stable isotope composition of tuna to provide a first insight into the existence of global trends in complex ecosystem dynamics and changes in the oceanic carbon cycle. From 2000 to 2015, considerable declines in δ13C values of 0.8‰–2.5‰ were observed across three tuna species sampled globally, with more substantial changes in the Pacific Ocean compared to the Atlantic and Indian Oceans. Tuna recorded not only the Suess effect, that is, fossil fuel‐derived and isotopically light carbon being incorporated into marine ecosystems, but also recorded profound changes at the base of marine food webs. We suggest a global shift in phytoplankton community structure, for example, a reduction in 13C‐rich phytoplankton such as diatoms, and/or a change in phytoplankton physiology during this period, although this does not rule out other concomitant changes at higher levels in the food webs. Our study establishes tuna δ13C values as a candidate essential ocean variable to assess complex ecosystem responses to climate change at regional to global scales and over decadal timescales. Finally, this time series will be invaluable in calibrating and validating global earth system models to project changes in marine biota.

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“…Changes in tuna δ 13 C values can in turn be described by the following equation:

{normalδ}^{13} {normalC}_{tuna} = \frac{1}{()(, 1 + \frac{ε_{fc}}{1, 000})} ({normalδ}^{13} {normalC}_{normalp} - ε_{fc}),

Section: Methodsmentioning

confidence: 99%

Trends in tuna carbon isotopes suggest global changes in pelagic phytoplankton communities

Lorrain

Pethybridge

Cassar

et al. 2019

Global Change Biology

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“… Caution is therefore needed when using SI values from the literature because the pre‐treatments vary widely between studies; the compared SI data thus reflect the intrinsic differences in the tissue composition combined with the influence of the pre‐treatments which may confound ecological interpretation; Our study, conducted on a limited number of samples, shows that the difference among pre‐treatments extends beyond the elasmobranch species and should therefore be confirmed with tests on additional species; The pre‐treatment comparative approach that we followed for ragged‐tooth sharks and Cape knifejaws could be adapted for other species prior to large scale studies to provide conversion factors; The next step would entail the evaluation of the pre‐treatments in their abilities in removing solely the biological molecules of interest (urea, TMAO, lipids). This would allow us to choose the best pre‐treatment which interferes least with the amino acid composition; We reiterate the call for a standardised approach to pre‐treatments which would greatly benefit larger‐scale comparisons of SI studies, particularly when global comparisons of wide‐ranging species are starting to emerge (e.g …”

Section: Resultsmentioning

confidence: 99%

“…This is likely to affect carbon and nitrogen contents and δ 13 C and δ 15 N values, as well as C:N ratios. Critically important information for comparisons between studies (e.g …”

Section: Introductionmentioning

confidence: 99%

Effects of pre‐treatments on bulk stable isotope ratios in fish samples: A cautionary note for studies comparisons

Connan

Hall

Smale

2019

Rapid Comm Mass Spectrometry

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Rationale Stable isotope analysis (SIA) has revolutionised ecological studies over the past thirty years. One of the major fields where SIA is applied in the marine environment is related to the definition of ecosystem structure and function. With marine top predators such as sharks, SIA is a method of choice because tissue samples can be collected without the sacrifice of the animal. In elasmobranch research, the influence of compounds such as urea, trimethylamine oxide and lipids must be considered when using stable isotopes as ecological markers. Currently, a range of pre‐treatments are used to chemically remove these molecules prior to SIA. Methods This study investigated the impact of eleven commonly used pre‐treatments on carbon and nitrogen contents and C:N atomic ratio, as well as carbon and nitrogen SI ratios in elasmobranch tissues and its prey, measured by isotope ratio mass spectrometry. Three tissues were tested: blood and muscle of the ragged‐tooth shark Carcharias taurus, and muscle of one teleost species, the Cape knifejaw Oplegnathus conwayi. Results Compared with untreated samples, no trend or generalisation could be highlighted with the influence of pre‐treatments being species‐, tissue‐ and chemical‐element‐dependent. For the δ13C and δ15N values, differences among pre‐treatments were as high as 3‰, therefore potentially leading to erroneous ecological interpretation. Conclusions The chemical properties of compounds (e.g. urea, lipids) combined with the polarity of solutions (e.g. water, solvents) explained a large part of these observations. This study highlights that pre‐treatments need to be considered especially when comparing carbon and nitrogen stable isotope ratios between studies. The results of this study provide a call to all stable isotope researchers to make a concerted effort to standardise pre‐treatment methods. This is crucial as global reviews are becoming increasingly more informative.

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“…A recent study utilizing carbon and nitrogen stable isotope ratios (δ 13 C and δ 15 N) suggested that Winter Skate individuals may predominantly forage within a specific latitudinal range (Shipley et al, in press), a pattern that has also been hypothesized for oceanic sharks (Bird et al. ). This result suggests that high rates of movement, particularly off coastal New York and New Jersey, could reflect primary foraging grounds laying outside of the immediate capture and tagging region.…”

Section: Discussionmentioning

confidence: 96%

First Observations of Long‐Distance Migration in a Large Skate Species, the Winter Skate: Implications for Population Connectivity, Ecosystem Dynamics, and Management

et al. 2019

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The overexploitation and decline of groundfish populations throughout the 1980s and 1990s resulted in a regime shift on Georges Bank and southern New England, which was characterized by subsequent exponential increases in the observed biomass of Winter Skate Leucoraja ocellata in the region. Recent work suggested that the rate of the Winter Skate biomass increase cannot be fully explained by internal population dynamics of a population without immigration from other regions and/or populations and that adult‐mediated population connectivity (AMPC) with neighboring regions is required to fully explain biomass trends. Despite this, no evidence of long‐distance dispersal has been observed for Winter Skate, with individuals assumed to display high endemicity to specific regions of the continental shelf. Annual movements of 58 Winter Skate captured off coastal New York were examined using passive acoustic telemetry, revealing seasonal long‐distance dispersal capabilities exceeding 1,000 km. In total, 88,783 unique acoustic detections were observed. Telemetered individuals had an average time at liberty of 199.73 d and collectively traveled 17,576.9 km. Individuals tended to migrate south during summer/fall and north during winter/spring. Movement rates of individuals averaged 9.88 km/d (95% confidence interval = 9.25–10.92 km/d) but ranged from 0.13 to 41.38 km/d. An additional 51 recaptured Winter Skate from a total of 3,416 marked with Floy tags suggested greater offshore movement than was observed in acoustically tagged individuals. Our results illustrate that the Winter Skate is a highly mobile species that moves extensively throughout its large geographic range, consistent with its observed ability to rapidly invade neighboring habitat via AMPC. This study has important implications for our understanding of the role of Winter Skate in northwest Atlantic communities and for management strategies therein.

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A global perspective on the trophic geography of sharks

Cited by 101 publications

References 43 publications

Trends in tuna carbon isotopes suggest global changes in pelagic phytoplankton communities

Trends in tuna carbon isotopes suggest global changes in pelagic phytoplankton communities

Effects of pre‐treatments on bulk stable isotope ratios in fish samples: A cautionary note for studies comparisons

First Observations of Long‐Distance Migration in a Large Skate Species, the Winter Skate: Implications for Population Connectivity, Ecosystem Dynamics, and Management

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