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.

Nissei Foundation grant to Dr Wyatt et al.

The Nissei Foundation has awarded Dr Wyatt and colleagues a Grant for Environmental Issues Research by Young Researchers, 環境問題研究助成 (若手研究):

Title: Elucidating jungle-to-reef connections using state-of-the-art chemical tracers: Towards harmony between human activities and the pristine environments of Iriomote-jima, Japan | 最先端化学トレーサーによる亜熱帯林とサンゴ礁生態系のつながりの 解明:西表島の貴重な自然の保全と人間活動の調和に向けて

Participants: Alex. S.J. Wyatt, Toshi Nagata, Yusuke Yokoyama, Toshihiro Miyajima, James Leichter (Scripps)

This grant will facilitate ongoing work examining ecological links between oceanic and terrestrial processes in the pristine coral reef ecosystems of the west coast of Iriomote-jima.  Preliminary isotope tracer work has demonstrated that corals may be strongly dependent  on ancient carbon exported from the forested catchment feeding into Funauki Bay, which suggests that reef habitats across the bay may depend on the preservation of the intact upstream sub-tropical forest.

More info: http://www.nihonseimei-zaidan.or.jp/kankyo/04_jisseki.html

Thank you to the Nissei Foundation for their support.

 

New paper on amino acid isotope analysis (Ohkouchi et al., Organic Geochemsitry)

Advances in the application of amino acid nitrogen isotopic analysis in ecological and biogeochemical studies

Naohiko Ohkouchi1,*, Yoshito Chikaraishi1,13, Hilary G. Close2, Brian Fry3, Thomas Larsen4, Daniel J. Madigan5, Matthew D. McCarthy6, Kelton W. McMahon7, Toshi Nagata8, Yuichi I. Naito1,14, Nanako O. Ogawa1, Brian N. Popp9, Shawn Steffan10,11, Yoshinori Takano1, Ichiro Tayasu12, Alex S.J. Wyatt8, Yasuhiko T. Yamaguchi8,15, Yusuke Yokoyama8

1 Department of Biogeochemistry, Japan Agency for Marine-Earth Science and Technology, Japan; 2 Rosenstiel School of Marine and Atmospheric Science, University of Miami, USA3 Australian Rivers Institute, Griffith University, Australia; 4 Leibniz-Laboratory, University of Kiel, Germany; 5 Harvard University Center for the Environment, USA; 6 Department of Ocean Sciences, University of California, Santa Cruz, USA; 7 Graduate School of Oceanography, University of Rhode Island, USA; 8 Atmosphere and Ocean Research Institute, The University of Tokyo, Japan; 9 Department of Geology and Geophysics, University of Hawaii, USA; 10 US Department of Agriculture, Agricultural Research Service, USA; 11 Department of Entomology, University of Wisconsin-Madison, USA; 12 Research Institute of Humanity and Nature, Japan; 13 Present address: Institute of Low Temperature Science, Hokkaido University, Japan; 14 Present address: Nagoya University Museum, Japan; 15 Present address: Lake Biwa Environmental Research Institute, Japan

Compound-specific isotopic analysis of amino acids (CSIA-AA) has emerged in the last decade as a powerful approach for tracing the origins and fate of nitrogen in ecological and biogeochemical studies. This approach is based on the empirical observation that source amino acids (AAs) (i.e., phenylalanine), fractionate 15N very little (< 0.5‰) during trophic transfer, whereas trophic AAs (i.e., glutamic acid), are greatly (∼6–8‰) enriched in 15N during each trophic step. The differential fractionation of these two AA groups can provide a valuable estimate of consumer trophic position that is internally indexed to the baseline δ15N value of the integrated food web. In this paper, we critically review the analytical methods for determining the nitrogen isotopic composition of AAs by gas chromatography–isotope-ratio mass spectrometry. We also discuss methodological considerations for accurate trophic position assessment of organisms using CSIA-AA. We then discuss the advantages and challenges of the CSIA-AA approach using published case studies across a range of topics, including trophic position assessment in various ecosystems, reconstruction of ancient human diets, reconstruction of animal migration and environmental variability, and assessment of marine organic matter dynamics with new classification of microbial fractionation patterns. It is clear that the CSIA-AA approach can provide unique insight into the sources, cycling, and trophic modification of organic nitrogen as it flows through systems. However, this approach will be greatly improved through continued exploration into how biochemical, physiological, and ecological mechanisms affect isotopic fractionation of individual AAs. We end this review with a perspective on future work that will promote the evolution of the rapidly growing field of CSIA-AA.

Sumitomo Foundation grant to Dr Wyatt et al.

The Sumitomo Foundation has awarded an Environmenal Research Grant (環境研究助成) to Dr Wyatt and colleagues for their pioneering work on the environmental drivers of the structure and function of ‘twilight reefs’ (deep-water mesophotic coral ecosystems).

Title: A refuge for coral reef biodiversity: trophic function and reproduction in the twilight zone | 危機に瀕したサンゴ礁生物の避難場所:薄明帯の学際的解明による保全・再生の支援

Participants: Alex S.J. Wyatt, Toshihiro Miyajima, Toshi Nagata, James Leichter (Scripps), Satoshi Mitarai (OIST), Kazuhiko Sakai (U Ryukyu), Rob Toonen (U Hawaii).

More info: http://www.sumitomo.or.jp/html/kankyo/kantaisyo2016.htm

Thank you to the Sumitomo Foundation for their support.

 

Impacts of internal waves on the twilight zone @ ICRS 2016, Hawaii (Dr Wyatt)

Ecological and biogeochemical impacts of internal waves on mesophotic coral ecosystems: testing eddy correlation and isotope approaches, Iriomote, Japan

Alex S.J. Wyatt1*, Toshihiro Miyajima1, James J. Leichter2, Tohru Naruse3, Tomohiro Kuwae4, Shoji Yamamoto5, Naomi Satoh1, Toshi Nagata1

1Department of Chemical Oceanography, Atmosphere and Ocean Research Institute, The University of Tokyo, Kashiwa, Chiba, JAPAN
2Scripps Institution of Oceanography, University of California at San Diego, La Jolla, California, USA
3Tropical Biosphere Research Center, University of the Ryukyus, Taketomi, Japan
4Coastal and Estuarine Environment Research Group, Port and Airport Research Institute (PARI), Nagase, Yokosuka, JAPAN
5Department of Earth and Planetary Science, The University of Tokyo, Bunkyo-ku, Tokyo, Japan

While mesophotic coral ecosystems (MCE) may be protected or damped from disturbances impacting shallower reefs insufficient information is available on the environmental conditions supporting these ‘deep water refugia’. Nutrient inputs and recycling have rarely been quantified over MCE but may differ fundamentally to that of shallow counterparts due to the reduction in light and increasing reliance on oceanic nutrients, leading to increased heterotrophy over autotrophy at species and ecosystem levels and stronger links to oceanic processes. For instance, due to the depth of MCE relative to typical water column density stratification, internal waves may be a highly significant process depending on community aspect and exposure. Preliminary observations of MCE along a continuum of oceanic exposure in Funauki Bay, Iriomote, Japan indicate that ocean-exposed MCE are subject to semi-diurnal temperature oscillations of up to 4 C during summer (range 23 – 29 deg C), while inner MCE occur shallower in more turbid but stable environments. Oceanic exposure along the bay may determine both the distribution and function of spatially extensive, but relatively homogenous, communities dominated by Leptoseris sp. or Acropora ?horrida. Combining bulk and compound-specific stable isotope analyses, depth-specific radioisotope markers such as radiocarbon, and eddy correlation experiments in these habitat promises a useful approach for elucidating the functional importance of internal waves in the development and persistence of MCE at local to regional scales.

Dongsha Atoll Research Award (2016-2017) to Dr Wyatt and Prof Wang

Dr Wyatt has been awarded the Dongsha Atoll Research Award (2016-2017) by the Dongsha Atoll Research Station (DARS), managed by Taiwan’s National Sun Yat-sen University (NSYU).  The award will facilitate the implementation of a collaborative project with Professor Yu-Huai Wang (NSYU) examining the impact of internal waves on the biochemistry and ecology of Dongsha’s reef communities, focusing on ‘twilight zone’ mesophotic coral ecosystems around the atoll.

Dr Wyatt is excited to begin examining the reefs around Dongsha Atoll, which experiences some of the most energetic internal wave activity on the planet, and collaborating with Professor Wang’s group and NSYU.  The support of the Dongsha Atoll Research Station is greatly appreciated.

Ecosystem inputs and recycling over coral reefs @ 3rd APCRS, 2014 (Dr Wyatt)

Functional understanding of ecosystem-scale inputs and recycling over coral reef communities from stable isotope analyses of organic matter

Alex S.J. Wyatt1*, James J. Leichter2, Benoit Thibodeau1, Toshihiro Miyajima1, Craig A. Carlson3, Craig E. Nelson4, Toshi Nagata1

1Marine Biogeochemistry Laboratory, Department of Chemical Oceanography, Atmosphere & Ocean Research Institute, The University of Tokyo, Kashiwa, Chiba, JAPAN
2Scripps Institution of Oceanography, University of California at San Diego, La Jolla, California, USA
3University of California at Santa Barbara, Santa Barbara, California, USA
4Center for Microbial Oceanography: Research and Education, University of Hawai’i, USA

Stable isotope analyses (SIA) are an increasingly useful tool for understanding functional links between water flow and nutrient cycling over coral reefs, including relative fluxes of oceanic and reef-derived material. SIA have suggested that oceanic particulate organic matter (POM) flowing over reefs can be rapidly metabolized, with the subsequent release of remineralized inorganic nutrients, as well reef-derived POM, representing a significant resource for downstream communities. High oceanic concentrations of dissolved organic matter (DOM) relative to POM suggests DOM may be an even more significant resource, especially around low-POM reefs such as mid-ocean islands and atolls. However, DOM fluxes have rarely been quantified, perhaps due to the refractory nature of oceanic DOM and difficulties linking small concentration changes with spatial changes in both hydrodynamics and macro- and microbial communities. Our Lagrangian studies of DOM around Moorea, French Polynesia and Ishigaki Island, Japan suggest that DOM changes occurring over short spatial scales reflect a balance between uptake and release. SIA further suggest that the release of reef-derived DOM (i.e. enriched in 13C), perhaps relatively labile and from nitrogen fixing organisms (i.e. depleted in 15N), may promote nutrient recycling and supply to downstream communities. Linking SIA and local hydrodynamics offers a promising path towards elucidating the relative functional importance of oceanic and reef-level processes for reef communities.

Key words: dissolved organic matter, fluxes, particulate organic matter, recycling, stable isotope analyses