Sharks are a diverse group of mobile predators that forage across varied spatial scales and have the potential to influence food web dynamics. The ecological consequences of recent declines in shark biomass may extend across broader geographic ranges if shark taxa display common behavioural traits. By tracking the original site of photosynthetic fixation of carbon atoms that were ultimately assimilated into muscle tissues of 5,394 sharks from 114 species, we identify globally consistent biogeographic traits in trophic interactions between sharks found in different habitats. We show that populations of shelf-dwelling sharks derive a substantial proportion of their carbon from regional pelagic sources, but contain individuals that forage within additional isotopically diverse local food webs, such as those supported by terrestrial plant sources, benthic production and macrophytes. In contrast, oceanic sharks seem to use carbon derived from between 30° and 50° of latitude. Global-scale compilations of stable isotope data combined with biogeochemical modelling generate hypotheses regarding animal behaviours that can be tested with other methodological approaches.
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Ebert, D. A., Fowler, S. L., Compagno, L. J. & Dando, M. Sharks of the World: A Fully Illustrated Guide (Wild Nature Press, Plymouth, 2013).
Ferretti, F., Worm, B., Britten, G. L., Heithaus, M. R. & Lotze, H. K. Patterns and ecosystem consequences of shark declines in the ocean. Ecol. Lett. 13, 1055–1071 (2010).
Worm, B. et al. Global catches, exploitation rates, and rebuilding options for sharks. Mar. Policy 40, 194–204 (2013).
Dulvy, N. K. et al. Extinction risk and conservation of the world’s sharks and rays. eLife 3, 1–34 (2014).
Kitchell, J. F., Essington, T. E., Boggs, C. H., Schindler, D. E. & Walters, C. J. The role of sharks and longline fisheries in a pelagic ecosystem of the central Pacific. Ecosystems 5, 202–216 (2002).
Myers, R. A., Baum, J. K., Shepherd, T. D., Powers, S. P. & Peterson, C. H. Cascading effects of the loss of apex predatory sharks from a coastal ocean. Science 315, 1846–1850 (2007).
Heithaus, M. R., Frid, A., Wirsing, A. J. & Worm, B. Predicting ecological consequences of marine top predator declines. Trends Ecol. Evol. 23, 202–210 (2008).
Heupel, M. R., Knip, D. M., Simpfendorfer, C. A. & Dulvy, N. K. Sizing up the ecological role of sharks as predators. Mar. Ecol. Prog. Ser. 495, 291–298 (2014).
Grubbs, R. D. et al. Critical assessment and ramifications of a purported marine trophic cascade. Sci. Rep. 6, 20970 (2016).
Roff, G. et al. The ecological role of sharks on coral reefs. Trends Ecol. Evol. 31, 395–407 (2016).
Ruppert, J. L., Fortin, M.-J. & Meekan, M. G. The ecological role of sharks on coral reefs: Response to Roff et al. Trends Ecol. Evol. 8, 586–587 (2016).
McCann, K., Hastings, A. & Huxel, G. R. Weak trophic interactions and the balance of nature. Nature 395, 794–798 (1998).
Fry, B. & Sherr, E. B. in Stable Isotopes in Ecological Research (eds Rundel, P. W., Ehleringer, J. R. & Nagy, K. A.) 196–229 (Springer, New York, 1989).
Laws, E. A., Popp, B. N., Bidigare, R. R., Kennicutt, M. C. & Macko, S. A. Dependence of phytoplankton carbon isotopic composition on growth rate and [CO2]aq: Theoretical considerations and experimental results. Geochim. Cosmochim. Acta 59, 1131–1138 (1995).
McMahon, K. W., Hamady, L. L. & Thorrold, S. R. A review of ecogeochemistry approaches to estimating movements of marine animals. Limnol. Oceanogr. 58, 697–714 (2013).
Hobson, K. A. Tracing origins and migration of wildlife using stable isotopes: a review. Oecologia 120, 314–326 (1999).
Magozzi, S., Yool, A., Vander Zanden, H. B., Wunder, M. B. & Trueman, C. N. Using ocean models to predict spatial and temporal variation in marine carbon isotopes. Ecosphere 8, e01763 (2017).
Cortés, E. Standardized diet compositions and trophic levels of sharks. ICES J. Mar. Sci. 56, 707–717 (1999).
Trueman, C. N., Johnston, G., O’Hea, B. & MacKenzie, K. M. Trophic interactions of fish communities at midwater depths enhance long-term carbon storage and benthic production on continental slopes. Proc. R. Soc. B 281, 20140669 (2014).
Briand, M. J., Bonnet, X., Guillou, G. & Letourneur, Y. Complex food webs in highly diversified coral reefs: insights from δ13C and δ15N stable isotopes. Food Webs 8, 12–22 (2016).
Kim, S. L., del Rio, C. M., Casper, D. & Koch, P. L. Isotopic incorporation rates for shark tissues from a long-term captive feeding study. J. Exp. Biol. 215, 2495–2500 (2012).
McMahon, K. W., Thorrold, S. R., Houghton, L. A. & Berumen, M. L. Tracing carbon flow through coral reef food webs using a compound-specific stable isotope approach. Oecologia 180, 809–821 (2016).
Chapman, D. D., Feldheim, K. A., Papastamatiou, Y. P. & Hueter, R. E. There and back again: a review of residency and return migrations in sharks, with implications for population structure and management. Annu. Rev. Mar. Sci. 7, 547–570 (2015).
Lea, J. S. et al. Repeated, long-distance migrations by a philopatric predator targeting highly contrasting ecosystems. Sci. Rep. 5, p11202 (2015).
Camhi, M. D., Pikitch, E. K. & Babcock, E. A. (eds) Sharks of the Open Ocean: Biology, Fisheries and Conservation (Blackwell, Oxford, 2008).
Ichii, T., Mahapatra, K., Sakai, M. & Okada, Y. Life history of the neon flying squid: effect of the oceanographic regime in the North Pacific Ocean. Mar. Ecol. Prog. Ser. 378, 1–11 (2009).
Scales, K. L. et al. On the front line: frontal zones as priority at-sea conservation areas for mobile marine vertebrates. J. Appl. Ecol. 51, 1575–1583 (2014).
Queiroz, N. et al. Ocean-wide tracking of pelagic sharks reveals extent of overlap with longline fishing hotspots. Proc. Natl Acad. Sci. USA 113, 1582–1587 (2016).
Tittensor, D. P. et al. Global patterns and predictors of marine biodiversity across taxa. Nature 466, 1098–1101 (2010).
Block, B. A. et al. Tracking apex marine predator movements in a dynamic ocean. Nature 475, 86–90 (2011).
Hazen, E. L. et al. Predicted habitat shifts of Pacific top predators in a changing climate. Nat. Clim. Chang. 3, 234–238 (2013).
Campana, S. E. et al. Migration pathways, behavioural thermoregulation and overwintering grounds of blue sharks in the northwest Atlantic. PLoS ONE 6, e16854 (2011).
Compagno, L. J. Sharks of the World: An Annotated and Illustrated Catalogue of Shark Species Known to Date Vol. 2 (Food & Agriculture Organization, Rome, 2001).
Moura, T. et al. Large-scale distribution of three deep-water squaloid sharks: integrating data on sex, maturity and environment. Fish. Res. 157, 47–61 (2014).
Veríssimo, A., McDowell, J. R. & Graves, J. E. Population structure of a deep-water squaloid shark, the Portuguese dogfish (Centroscymnus coelolepis). ICES J. Mar. Sci. 68, 555–563 (2011).
Rodríguez-Cabello, C., González-Pola, C. & Sánchez, F. Migration and diving behavior of Centrophorus squamosus in the NE Atlantic. Combining electronic tagging and Argo hydrography to infer deep ocean trajectories. Deep-Sea Res. 115, 48–62 (2016).
Heupel, M. & Simpfendorfer, C. Importance of environmental and biological drivers in the presence and space use of a reef-associated shark. Mar. Ecol. Prog. Ser. 496, 47–57 (2014).
Edgar, G. J. et al. Global conservation outcomes depend on marine protected areas with five key features. Nature 506, 216–220 (2014).
Heupel, M. R. et al. Conservation challenges of sharks with continental scale migrations. Front. Mar. Sci. 2, 12 (2015).
White, T. D. et al. Assessing the effectiveness of a large marine protected area for reef shark conservation. Biol. Conserv. 207, 64–71 (2017).
Borrell, A., Aguilar, A., Gazo, M., Kumarran, R. P. & Cardona, L. Stable isotope profiles in whale shark (Rhincodon typus) suggest segregation and dissimilarities in the diet depending on sex and size. Environ. Biol. Fishes 92, 559–567 (2011).
Hussey, N. E. et al. Expanded trophic complexity among large sharks. Food Webs 4, 1–7 (2015).
Maljković, A. & Côté, I. M. Effects of tourism-related provisioning on the trophic signatures and movement patterns of an apex predator, the Caribbean reef shark. Biol. Conserv. 144, 859–865 (2011).
Matich, P., Heithaus, M. R. & Layman, C. A. Contrasting patterns of individual specialization and trophic coupling in two marine apex predators. J. Anim. Ecol. 80, 294–305 (2011).
Kiljunen, M. et al. A revised model for lipid-normalizing δ13C values from aquatic organisms, with implications for isotope mixing models. J. Appl. Ecol. 43, 1213–1222 (2006).
This research was conducted as part of C.S.B.’s Ph.D dissertation, which was funded by the University of Southampton and NERC (NE/L50161X/1), and through a NERC Grant-in-Kind from the Life Sciences Mass Spectrometry Facility (LSMSF; EK267-03/16). We thank A. Bates, D. Sims, F. Neat, R. McGill and J. Newton for their analytical contributions and comments on the manuscripts.
The authors declare no competing financial interests.
Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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