Global analysis reveals how sharks travel the oceans to find food

A major international collaboration, including AORI researcher Dr. Alex Wyatt and authors from 20 other countries, could help global efforts to overturn recent declines in the world’s shark population by providing greater insight into the feeding habits of the world’s most misunderstood fish.

Led by Dr. Christopher Bird from the University of Southampton, the study published in Nature Ecology & Evolution, used chemical markers in the form of carbon isotopes found in sharks to investigate where in the world they have been feeding – an unresolved question for many shark species. Knowing which parts of the global ocean are important shark feeding areas may help to design more effective conservation measures to protect declining shark populations.

Distribution of compiled shark data and plankton isotopes from Bird et al. (2018) Nature Ecology & Evolution.

All life depends on carbon at the bottom of the food chain. Carbon comes in three forms or isotopes, and the proportions of two of the most common isotopes vary across the world’s ocean. In the study, 73 scientists from 21 countries compared the carbon isotopes from more than 5000 sharks from 114 species across the globe with those from phytoplankton at the bottom of the food web.

“If an animal feeds in the same place where it was caught, the carbon isotope signals in the shark and phytoplankton will match.,” says Dr Bird whose PhD research was focused on deep-sea sharks. “However, if the shark has moved between feeding and where it was caught, then the signals will be different.

“You’ve heard of ‘you are what you eat’ – well this is more ‘you are where you ate’”

“You’ve heard of ‘you are what you eat’ – well this is more ‘you are where you ate’”, Bird continued. “We were able to show that sharks living close to land and those that live in the open ocean have very different ways of feeding.  The global study used muscle tissues to show that sharks living near to the coast feed locally across a range of different food webs –this is like people living in a city with access to lots of different restaurants in the neighbourhood and no need to travel far to find the food they want. On the other hand, oceanic sharks that are found throughout the world’s oceans, appear to get most of their food from specific areas of cooler water in the northern and southern hemispheres. This is more like travelling long distances from rural areas to spend lots of time eating in a few restaurants in a distant city.

“Our results suggest that for whale sharks, we can isotopically capture feeding that occurred in the months to years prior to sampling by sampling a range of slow and fast tissues, like blood plasma and fin cartilage, respectively”. Dr Wyatt added that future work looking at multiple tissues is expected to add a temporal dimension, “in this case, not only are ‘you what and where you ate’ but also ‘when you ate’”.

Carbon isotopes of different types of sharks from Bird et al. (2018) Nature Ecology & Evolution.

These findings are very important for Dr Wyatt, who is using isotopes to better understand the open ocean movements and foraging strategies of planktivorous sharks and rays like the whale shark.  “Our results from captive whale sharks, in collaboration with Okinawa Churaumi Aquarium, have demonstrated that we can use carbon isotopes measured in different tissues of one shark to show changes in feeding activity of that individual over time” says Dr Wyatt.

This is because different tissues have different rates of metabolic turnover, and can thus reflect feeding over different time scales.  “Our results suggest that for whale sharks, we can isotopically capture feeding that occurred in the months to years prior to sampling by sampling a range of slow and fast tissues, like blood plasma and fin cartilage, respectively”. Dr Wyatt added that future work looking at multiple tissues is expected to add a temporal dimension, “in this case, not only are ‘you what and where you ate’ but also ‘when you ate’”.

Such increased understanding of global shark feeding is considered vital for their conservation. “With over 500 known species around the world, sharks are certainly amongst our most diverse and misunderstood group of fish but we still have limited knowledge of their habits and behaviours, particularly relating to feeding and movement|” said Dr. Christopher Bird. “Over the last 50 years, the pressures of fishing and habitat degradation have resulted in declines amongst some of the world’s shark populations, the effects of which are also not fully understood.”

Cartoon summarising the research (credit: Clive Trueman)

Senior author Dr Clive Trueman, Associate Professor in Marine Ecology from the University of Southampton added, “The results have important implications for conservation. Globally, sharks are not doing well. Many shark populations have declined in the last few decades, particularly in the wide-ranging oceanic sharks that are targeted by fishing boats and caught accidentally in tuna fisheries as “by-catch”. Governments are now creating large marine protected areas around the globe, which help to reduce fishing, but most of these protected areas are in tropical waters, and may not provide effective protection for oceanic sharks.”

“Sharks urgently need our help, but to help them we also need to understand them. Our study has helped by identifying important shark feeding grounds. New technologies like satellite and isotope tracking are giving us the information we need to turn the tide on these beautiful and fascinating animals.”

The paper ‘A global perspective on the trophic geography of sharks’ is published in the February issue of Nature Ecology & Evolution (doi 10.1038.s41559-017-0432-z).


View the Nature blog post here:

https://goo.gl/BF73Uk

View the article here:

https://www.nature.com/articles/s41559-017-0432-z

View the cartoon here:

https://goo.gl/iS8voV

More information on the Chondrichthyan Stable Isotope Data Project (CSIDP):

https://goo.gl/Wmmzk3


 

New paper on the trophic geography of sharks (Bird et al., Nature Ecology & Evolution)

A global perspective on the trophic geography of sharks

Christopher S. Bird 1,71*, Ana Veríssimo2,3, Sarah Magozzi1, Kátya G. Abrantes4, Alex Aguilar5, Hassan Al-Reasi6, Adam Barnett4, Dana M. Bethea7,72, Gérard Biais8, Asuncion Borrell 5, Marc Bouchoucha9, Mariah Boyle10, Edward J. Brooks11, Juerg Brunnschweiler12, Paco Bustamante 13, Aaron Carlisle14, Diana Catarino 15, Stéphane Caut16, Yves Cherel17, Tiphaine Chouvelon18, Diana Churchill19, Javier Ciancio20, Julien Claes21, Ana Colaço15, Dean L. Courtney 22,73, Pierre Cresson23, Ryan Daly24,25, Leigh de Necker26, Tetsuya Endo27, Ivone Figueiredo28, Ashley J. Frisch29, Joan Holst Hansen30, Michael Heithaus31, Nigel E. Hussey32, Johannes Iitembu33, Francis Juanes34, Michael J. Kinney 35, Jeremy J. Kiszka 36, Sebastian A. Klarian37, Dorothée Kopp38, Robert Leaf39, Yunkai Li40, Anne Lorrain41, Daniel J. Madigan42, Aleksandra Maljković43, Luis Malpica-Cruz44, Philip Matich45,46, Mark G. Meekan47, Frédéric Ménard48, Gui M. Menezes15, Samantha E. M. Munroe49, Michael C. Newman50, Yannis P. Papastamatiou51,52, Heidi Pethybridge53, Jeffrey D. Plumlee54,55, Carlos Polo-Silva56, Katie Quaeck-Davies1, Vincent Raoult 57, Jonathan Reum58, Yassir Eden Torres-Rojas59, David S. Shiffman60, Oliver N. Shipley61, Conrad W. Speed47, Michelle D. Staudinger62,63, Amy K. Teffer64, Alexander Tilley 65, Maria Valls66, Jeremy J. Vaudo67, Tak-Cheung Wai68, R. J. David Wells54,55, Alex S. J. Wyatt 69, Andrew Yool70 and Clive N. Trueman1*

[Author affiliations]

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.

Adding to our isotope axes @ IsoEcol 2016 (Dr Wyatt)

Amino acid and radiocarbon insights from captive whale sharks

Alex S.J. WYATT1*, Rui Matsumoto2, Yoshito Chikaraishi3, Yosuke Miyari1, Yusuke Yokoyama1, Keiichi Sato2, Nao Ohkouchi3, Toshi Nagata1

1Atmosphere and Ocean Research Institute, The University of Tokyo, Kashiwa, Chiba, JAPAN
2Okinawa Churaumi Aquarium, Motobu, Okinawa, JAPAN
3Japan Agency for Marine-Earth Science and Technology, Yokosuka, JAPAN
*Presenting author

Stable isotope analyses (SIA) have the potential to provide novel insights into spatial and temporal patterns in the trophic ecology of poorly understood organisms like whale sharks Rhincodon typus. However, interpreting SIA depends on accurate diet-tissue discrimination factors (DTDF) to quantify diets and trophic positions, with experimental derivations of DTDF rare for such large-bodied organisms. Captive R. typus have provided a unique opportunity to validate a range of SIA, compound-specific isotope analyses (CSIA) and radioisotope approaches in the world’s largest fish and one of three planktivorous sharks. Diet records over the past five years revealed a diet dominated by North Pacific and Antarctic krill, 44% and 49% of weighted diet for Euphausia pacifica and E. superba, respectively. Despite the well-known diet, SIA of fin tissue from three captive R. typus (7.1, 7.2, and 8.4 m in length) proved hard to reconcile, especially for bulk carbon. In contrast, CSIA of amino acid (AA) nitrogen in the sharks’ tissue was relatively stable over time, despite evidence of variation in AA compositions and δ15N-AA of diet components. Tissue radiocarbon further suggested either long turnover in fin tissues (27 months), or the preferential assimilation of the smaller E. pacifica14C of 3 ‰ compared to -112 ‰ for E. superba). Daily-scale analysis of radiocarbon in R. typus faeces may support the preferential assimilation hypothesis, faeces generally being depleted relative to diet. Together, CSIA-AA and radiocarbon analyses add multiple addtional axes to our isotope space and may alleviate some of the complications involved in interpreting bulk SIA in ecological studies.

Reef fish trophodynamics (Wyatt et al., Coral Reefs)

Stable isotope analysis reveals community-level variation in fish trophodynamics across a fringing coral reef

A. S. J. Wyatt, A. M. Waite, S. Humphries

In contrast to trophodynamic variations, the marked zonation in physical and biological processes across coral reefs and the concomitant changes in habitat and community structure are well documented. In this study, we demonstrate consistent spatial changes in the community-level trophodynamics of 46 species of fish across the fringing Ningaloo Reef, Western Australia, using tissue stable isotope and fatty acid analyses. Increasing nitrogen (δ15N) and decreasing carbon (δ13C) isotope ratios in the tissues of herbivores, planktivores and carnivores with increasing proximity to the ocean were indicative of increased reliance on oceanic productivity. In contrast, detritivores and corallivores displayed no spatial change in δ15N or δ13C, indicative of the dependence on reef-derived material across the reef. Higher δ13C, as well as increased benthic- and bacterial-specific fatty acids, suggested reliance on reef-derived production increased in back-reef habitats. Genus-level analyses supported community- and trophic group-level trends, with isotope modelling of species from five genera (Abudefduf sexfasciatus, Chromis viridis, Dascyllus spp.,Pomacentrus spp. and Stegastes spp.), demonstrating declining access to oceanic zooplankton and, in the case of Pomacentrus spp. and Stegastes spp., a switch to herbivory in the back-reef. The spatial changes in fish trophodynamics suggest that the relative roles of oceanic and reef-derived nutrients warrant more detailed consideration in reef-level community ecology.

Reef fish discrimination (Wyatt et al., PLoS One)

Variability in Isotope Discrimination Factors in Coral Reef Fishes: Implications for Diet and Food Web Reconstruction

Alex S.J. Wyatt, Stuart Humphries, Anya M. Waite

Interpretation of stable isotope ratios of carbon and nitrogen (δ13C and δ15N) is generally based on the assumption that with each trophic level there is a constant enrichment in the heavier isotope, leading to diet-tissue discrimination factors of 3.4‰ for 15N (ΔN) and ~0.5‰ for13C (ΔC). Diet-tissue discrimination factors determined from paired tissue and gut samples taken from 152 individuals from 26 fish species at Ningaloo Reef, Western Australia demonstrate a large amount of variability around constant values. While caution is necessary in using gut contents to represent diet due to the potential for high temporal variability, there were significant effects of trophic position and season that may also lead to variability in ΔN under natural conditions. Nitrogen enrichment increased significantly at higher trophic levels (higher tissue δ15N), with significantly higher ΔN in carnivorous species. Changes in diet led to significant changes in ΔN, but not tissue δ15N, between seasons for several species:Acanthurus triostegus, Chromis viridis, Parupeneus signatus and Pomacentrus moluccensis. These results confirm that the use of meta-analysis averages for ΔN is likely to be inappropriate for accurately determining diets and trophic relationships using tissue stable isotope ratios. Where feasible, discrimination factors should be directly quantified for each species and trophic link in question, acknowledging the potential for significant variation away from meta-analysis averages and, perhaps, controlled laboratory diets and conditions.

Keywords: diet, food web, gut contents, mixing models, Ningaloo Reef, tissue isotopes