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Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE (Open Access)

Isotopic evidence of connectivity between an inshore vegetated lagoon (nursery habitat) and coastal artificial reefs (adult habitats) for the reef fish Lethrinus lentjan on the Terengganu coast, Malaysia

Dung Quang Le https://orcid.org/0000-0002-5951-6816 A E , Siau Yin Fui A , Rumeaida Mat Piah B , Toyoho Ishimura C , Yuji Sano D , Kentaro Tanaka D and Kotaro Shirai D
+ Author Affiliations
- Author Affiliations

A Institute of Oceanography and Environment, Universiti Malaysia Terengganu, 21030 Kuala Nerus, Terengganu, Malaysia.

B School of Fisheries and Aquaculture Sciences, Universiti Malaysia Terengganu, 21030 Kuala Nerus, Terengganu, Malaysia.

C Department of Industrial Engineering, National Institute of Technology, Ibaraki College, 866 Nakane, Hitachinaka, Ibaraki 312-8508 Japan.

D Atmosphere and Ocean Research Institute, The University of Tokyo, 5-1-5, Kashiwanoha, Kashiwa-shi, Chiba 277-8564 Japan.

E Corresponding author. Email: lqdungimer@gmail.com; le.dung@umt.edu.my

Marine and Freshwater Research 70(12) 1675-1688 https://doi.org/10.1071/MF18302
Submitted: 1 August 2018  Accepted: 1 May 2019   Published: 6 August 2019

Journal Compilation © CSIRO 2019 Open Access CC BY-NC-ND

Abstract

Stable isotope analyses of muscle tissue (δ13Cmuscle and δ15Nmuscle) and otoliths (δ13Cotolith and δ18Ootolith) were used to retrospectively track habitat uses of Lethrinus lentjan, and to determine any association between Setiu Lagoon (nursery habitat) and coastal artificial reefs (CARs; adult habitats) on the Terengganu coast, Malaysia. Muscle stable isotopes exhibited a spatial change from inshore to offshore habitats associated with growth, possibly related to the reef-ward movement of the fish. Otolith stable isotopes of adult fish from CARs were measured in juvenile (from outside the core to the first opaque zone of otolith) and adult (the edge of otolith) portions and were compared with those of juveniles from Setiu Lagoon, suggesting that the adult fish may not primarily use the lagoon as a nursery before ontogenetically migrating to CARs. The effects of coastal currents between monsoonal seasons could reorientate offshore juvenile migration; hence, adult cohorts in CARs may be replenished from various nursery habitats along the coast. Additionally, similarities in the δ18Ootolith values of juvenile and adult sections suggested that some individuals may not spend their juvenile phases in shallow estuarine habitats. Based on the findings of this study, we recommend that coastal conservation strategies take into account multiple nursery habitats rather than a single one.

Additional keywords: ecological linkage, muscle, otolith, stable isotopes.


References

Abrantes, K. G., Johnston, R., Connolly, R. M., and Sheaves, M. (2015). Importance of mangrove carbon for aquatic food webs in wet–dry tropical estuaries. Estuaries and Coasts 38, 383–399.
Importance of mangrove carbon for aquatic food webs in wet–dry tropical estuaries.Crossref | GoogleScholarGoogle Scholar |

Akhir, M. F. M. (2012). Surface circulation and temperature distribution of southern South China Sea from Global Ocean Model (OCCAM). Sains Malaysiana 41, 701–714.

Akhir, M. F. M., Zakaria, N. Z., and Tangang, F. (2014). Intermonsoon variation of physical characteristics and current circulation along the east coast of Peninsular Malaysia. International Journal of Oceanography 2014, 527587.
Intermonsoon variation of physical characteristics and current circulation along the east coast of Peninsular Malaysia.Crossref | GoogleScholarGoogle Scholar |

Ali, A., Abdullah, M. P., Hazizi, R., Marzuki, A. H., and Hassan, R. B. R. (2013). Protecting coastal habitats and enhancing fisheries resources using big size artificial reefs in the east coast of Peninsular Malaysia. Malaysian Journal of Science 32, 19–36.
Protecting coastal habitats and enhancing fisheries resources using big size artificial reefs in the east coast of Peninsular Malaysia.Crossref | GoogleScholarGoogle Scholar |

Amano, Y., Shiao, J., Ishimura, T., Yokouchi, K., and Shirai, K. (2015). Otolith geochemical analysis for stock discrimination and migratory ecology of tunas. In ‘Biology and Ecology of Bluefin Tuna’. (Eds T. Kitagawa, and S. Kimura.) Chapt. 10, pp. 225–257. (CRC Press: Boca Raton, FL, USA.)

Arney, R. N., Froehlich, C. Y. M., and Kline, R. J. (2017). Recruitment patterns of juvenile fish at an artificial reef area in the Gulf of Mexico. Marine and Coastal Fisheries 9, 79–92.
Recruitment patterns of juvenile fish at an artificial reef area in the Gulf of Mexico.Crossref | GoogleScholarGoogle Scholar |

Ashford, J., and Jones, C. (2007). Oxygen and carbon stable isotopes in otoliths record spatial isolation of Patagonian toothfish (Dissostichus eleginoides). Geochimica et Cosmochimica Acta 71, 87–94.
Oxygen and carbon stable isotopes in otoliths record spatial isolation of Patagonian toothfish (Dissostichus eleginoides).Crossref | GoogleScholarGoogle Scholar |

Barnett, V., and Lewis, T. (1994). ‘Outliers in Statistical Data’, 3rd edn. (Wiley: New York, NY, USA.)

Bastow, T. P., Jackson, G., and Edmonds, J. S. (2002). Elevated salinity and isotopic composition of fish otolith carbonate: stock delineation of pink snapper, Pagrusauratus, in Shark Bay, Western Australia. Marine Biology 141, 801–806.
Elevated salinity and isotopic composition of fish otolith carbonate: stock delineation of pink snapper, Pagrusauratus, in Shark Bay, Western Australia.Crossref | GoogleScholarGoogle Scholar |

Berkström, C., Gullstrom, M., Lindborg, G., Mwandya, A. W., Yahya, S. A., Kautsky, N., and Nystrom, M. (2012). Exploring ‘knowns’ and ‘unknowns’ in tropical seascape connectivity with insights from East African coral reefs. Estuarine, Coastal and Shelf Science 107, 1–21.
Exploring ‘knowns’ and ‘unknowns’ in tropical seascape connectivity with insights from East African coral reefs.Crossref | GoogleScholarGoogle Scholar |

Berkström, C., Jörgensen Lund, T., and Hellström, M. (2013). Ecological connectivity and niche differentiation between two closely related fish species in the mangroves-seagrass-coral reef continuum. Marine Ecology Progress Series 477, 201–215.
Ecological connectivity and niche differentiation between two closely related fish species in the mangroves-seagrass-coral reef continuum.Crossref | GoogleScholarGoogle Scholar |

Blacker, R. W. (1974). Recent advances in otolith studies. In ‘Sea Fisheries Research’. (Ed. F. R. H. Jones.) pp. 67–90. (Wiley: New York, NY, USA.)

Bohnsack, J. A. (1989). Are high densities of fishes at artificial reefs the result of habitat limitation or behavioral preference? Bulletin of Marine Science 44, 631–645.

Bouillon, S., Connolly, R. M., and Gillikin, D. P. (2011). Use of stable isotopes to understand food webs and ecosystem functioning in estuaries. In ‘Treatise on Estuarine and Coastal Science’. (Eds E. Wolanski and D. S. McLusky.) Chapt. 7, pp. 143–173. (Academic Press: Waltham, MA, USA.)

Bowen, G. J. (2010). Isoscapes: spatial pattern in isotopic biogeochemistry. Annual Review of Earth and Planetary Sciences 38, 161–187.
Isoscapes: spatial pattern in isotopic biogeochemistry.Crossref | GoogleScholarGoogle Scholar |

Brazner, J. C., Campana, S. E., Tanner, D. K., and Schram, S. T. (2004). Reconstructing habitat use and wetland nursery origin of yellow perch from Lake Superior using otolith elemental analysis. Journal of Great Lakes Research 30, 492–507.
Reconstructing habitat use and wetland nursery origin of yellow perch from Lake Superior using otolith elemental analysis.Crossref | GoogleScholarGoogle Scholar |

Burke, L., Reytar, K., Spalding, M., and Perry, A. (2012). Reefs at risk revisited in the coral triangle. (World Resources Institute: Washington, DC, USA.) Available at http://www.wri.org/our-work/project/reefs-risk/reefs-risk-revisited-coral-triangle-2012 [Verified 6 June 2019].

Campana, S. E. (1999). Chemistry and composition of fish otolith; pathways, mechanisms and applications. Marine Ecology Progress Series 188, 263–297.
Chemistry and composition of fish otolith; pathways, mechanisms and applications.Crossref | GoogleScholarGoogle Scholar |

Campana, S. E., and Thorrold, S. (2001). Otoliths, increments, and elements: keys to a comprehensive understanding of fish populations? Canadian Journal of Fisheries and Aquatic Sciences 58, 30–38.
Otoliths, increments, and elements: keys to a comprehensive understanding of fish populations?Crossref | GoogleScholarGoogle Scholar |

Carpenter, K. E., Lawrence, A., and Myers, R. (2016). Pinkear emperor Lethrinus lentjan. In ‘The IUCN Red List of Threatened Species 2016’. e.T16720036A16722340. (International Union for Conservation of Nature and Natural Resources.) https://www.iucnredlist.org/species/16720036/16722340 [Verified 6 June 2019].

Carr, M. H., Robinson, S. P., Wahle, C., Davis, G., Kroll, S., Murray, S., Schumacker, E. J., and Williams, M. (2017). The central importance of ecological spatial connectivity to effective coastal marine protected areas and to meeting the challenges of climate change in the marine environment. Aquatic Conservation 27, 6–29.
The central importance of ecological spatial connectivity to effective coastal marine protected areas and to meeting the challenges of climate change in the marine environment.Crossref | GoogleScholarGoogle Scholar |

Cocheret de la Morinière, E., Pollux, B. J. A., Nagelkerken, I., Hemminga, M. A., Huiskes, A. H. L., and van der Velde, G. (2003). Ontogenetic dietary changes of coral reef fishes in the mangrove–seagrass–reef continuum: stable isotopes and gut-content analysis. Marine Ecology Progress Series 246, 279–289.
Ontogenetic dietary changes of coral reef fishes in the mangrove–seagrass–reef continuum: stable isotopes and gut-content analysis.Crossref | GoogleScholarGoogle Scholar |

Craig, H. (1961). Isotopic variations in meteoric waters. Science 133, 1702–1703.
Isotopic variations in meteoric waters.Crossref | GoogleScholarGoogle Scholar | 17814749PubMed |

Cresson, P., Ruitton, S., and Harmelin-Vivien, M. (2014). Artificial reefs do increase secondary biomass production: mechanisms evidenced by stable isotopes. Marine Ecology Progress Series 509, 15–26.
Artificial reefs do increase secondary biomass production: mechanisms evidenced by stable isotopes.Crossref | GoogleScholarGoogle Scholar |

Cruz-Trinidad, A., Aliño, P. M., Geronimo, R. C., and Cabral, R. B. (2014). Linking food security with coral reefs and fisheries in the coral triangle Coastal Management 42, 160–182.
Linking food security with coral reefs and fisheries in the coral triangleCrossref | GoogleScholarGoogle Scholar |

Dansgaard, W. (1964). Stable isotopes in precipitation. Tellus 16, 436–468.
Stable isotopes in precipitation.Crossref | GoogleScholarGoogle Scholar |

Daryabor, F., Samah, A. A., and Ooi, S. H. (2015). Dynamical structure of the sea off the east coast of Peninsular Malaysia. Ocean Dynamics 65, 93–106.
Dynamical structure of the sea off the east coast of Peninsular Malaysia.Crossref | GoogleScholarGoogle Scholar |

Davis, J. P., Pitt, K. A., Fry, B., and Connoly, R. M. (2015). Stable isotopes as tracers of residency for fish on inshore coral reefs. Estuarine, Coastal and Shelf Science 167, 368–376.
Stable isotopes as tracers of residency for fish on inshore coral reefs.Crossref | GoogleScholarGoogle Scholar |

Delaygue, G., Bard, E., Rollion, C., Jouzel, J., Stievenard, M., Duplessy, J. C., and Ganssen, G. (2001). Oxygen isotope/salinity relationship in the northern Indian Ocean. Journal of Geophysical Research 106, 4565–4574.
Oxygen isotope/salinity relationship in the northern Indian Ocean.Crossref | GoogleScholarGoogle Scholar |

Dupont, J. M. (2008). Artificial reefs as restoration tools: a case study on the West Florida Shelf. Coastal Management 36, 495–507.
Artificial reefs as restoration tools: a case study on the West Florida Shelf.Crossref | GoogleScholarGoogle Scholar |

Edmonds, J. S., Steckis, R. A., Moran, M. J., Caputi, N., and Morita, M. (1999). Stock delineation of pink snapper and tailor from Western Australia by analysis of stable isotope and strontium/calcium ratios in otolith carbonate. Journal of Fish Biology 55, 243–259.
Stock delineation of pink snapper and tailor from Western Australia by analysis of stable isotope and strontium/calcium ratios in otolith carbonate.Crossref | GoogleScholarGoogle Scholar |

Elsdon, T. S., and Gillanders, B. M. (2002). Interactive effects of temperature and salinity on otolith chemistry: challenges for determining environmental histories of fish. Canadian Journal of Fisheries and Aquatic Sciences 59, 1796–1808.
Interactive effects of temperature and salinity on otolith chemistry: challenges for determining environmental histories of fish.Crossref | GoogleScholarGoogle Scholar |

Elsdon, T. S., Wells, B. K., Campana, S. E., Gillandres, B. M., Jones, C. M., Limburg, K. E., Secor, D. H., Thorrold, S. R., and Walther, B. D. (2008). Otolith chemistry to describe movements and life history parameters of fishes; hypotheses, assumptions, limitations and inferences. Oceanography and Marine Biology – an Annual Review 46, 297–330.
Otolith chemistry to describe movements and life history parameters of fishes; hypotheses, assumptions, limitations and inferences.Crossref | GoogleScholarGoogle Scholar |

Elsdon, T. S., Ayvazian, S., McMahon, K. W., and Thorrold, S. R. (2010). Experimental evaluation of stable isotope fractionation in fish muscle and otoliths. Marine Ecology Progress Series 408, 195–205.
Experimental evaluation of stable isotope fractionation in fish muscle and otoliths.Crossref | GoogleScholarGoogle Scholar |

Estudillo, C. B., Duray, M. N., Marasigan, E. T., and Emata, A. C. (2000). Salinity tolerance of larvae of the mangrove red snapper (Lutjanus argentimaculatus) during ontogeny. Aquaculture 190, 155–167.
Salinity tolerance of larvae of the mangrove red snapper (Lutjanus argentimaculatus) during ontogeny.Crossref | GoogleScholarGoogle Scholar |

Fry, B. (2008). ‘Stable Isotope Ecology’, 3rd edn. (Springer Science+Business Media, LLC: New York, NY, USA.)

Fry, B., and Sherr, E. B. (1984). δ13C measurements as indicators of carbon flow in marine and freshwater ecosystems Contributions in Marine Science 27, 13–47.

Gao, Y., Bargmann, G. G., Brand, U., and Noakes, D. L. G. (2005). Stable isotopic and trace elemental compositions of otoliths and the stock structure of Pacific cod, Gadus macrocephalus. Environmental Biology of Fishes 74, 335–348.
Stable isotopic and trace elemental compositions of otoliths and the stock structure of Pacific cod, Gadus macrocephalus.Crossref | GoogleScholarGoogle Scholar |

Grandcourt, E., Al Abdessalaam, T. Z., Francis, F., and Al Shamsi, A. (2011). Demographic parameters and status assessments of Lutjanus ehrenbergii, Lethrinus lentjan, Plectorhinchus sordidus and Rhabdosargus sarba in the southern Arabian Gulf. Journal of Applied Ichthyology 27, 1203–1211.
Demographic parameters and status assessments of Lutjanus ehrenbergii, Lethrinus lentjan, Plectorhinchus sordidus and Rhabdosargus sarba in the southern Arabian Gulf.Crossref | GoogleScholarGoogle Scholar |

Herzka, S. Z. (2005). Assessing connectivity of estuarine fishes based on stable isotope ratio analysis. Estuarine, Coastal and Shelf Science 64, 58–69.
Assessing connectivity of estuarine fishes based on stable isotope ratio analysis.Crossref | GoogleScholarGoogle Scholar |

Honda, K., Nakamura, Y., Nakaoka, M., Uy, W. H., and Fortes, M. D. (2013). Habitat use by fishes in coral reefs, seagrass beds and mangrove habitats in the Philippines. PLoS One 8, e65735.
Habitat use by fishes in coral reefs, seagrass beds and mangrove habitats in the Philippines.Crossref | GoogleScholarGoogle Scholar | 24312621PubMed |

Huijbers, C. M., Nagelkerken, I., and Layman, C. A. (2015). Fish movement from nursery bays to coral reefs: a matter of size? Hydrobiologia 750, 89–101.
Fish movement from nursery bays to coral reefs: a matter of size?Crossref | GoogleScholarGoogle Scholar |

Huxham, M., Kimuni, E., Newton, J., and Augley, J. (2007). Stable isotope records from otoliths as tracers of fish migration in a mangrove system. Journal of Fish Biology 70, 1554–1567.
Stable isotope records from otoliths as tracers of fish migration in a mangrove system.Crossref | GoogleScholarGoogle Scholar |

Jamieson, R. E., Schwarcz, H. P., and Brattey, J. (2004). Carbon isotopic records from the otoliths of Atlantic cod (Gadus morhua) from eastern Newfoundland, Canada. Fisheries Research 68, 83–97.
Carbon isotopic records from the otoliths of Atlantic cod (Gadus morhua) from eastern Newfoundland, Canada.Crossref | GoogleScholarGoogle Scholar |

Jensen, A. (2002). Artificial reefs of Europe: perspective and future. ICES Journal of Marine Science 59, S3–S13.
Artificial reefs of Europe: perspective and future.Crossref | GoogleScholarGoogle Scholar |

Kalish, J. M. (1991). 13C and 18O isotopic disequilibria in fish otoliths: metabolic and kinetic effects. Marine Ecology Progress Series 75, 191–203.
13C and 18O isotopic disequilibria in fish otoliths: metabolic and kinetic effects.Crossref | GoogleScholarGoogle Scholar |

Kerr, L. A., Secor, D. H., and Kraus, R. T. (2007). Stable isotope (δ13C and δ18O) and Sr/Ca composition of otoliths as proxies for environmental salinity experienced by an estuarine fish. Marine Ecology Progress Series 349, 245–253.
Stable isotope (δ13C and δ18O) and Sr/Ca composition of otoliths as proxies for environmental salinity experienced by an estuarine fish.Crossref | GoogleScholarGoogle Scholar |

Kim, S. T., Mucci, A., and Taylor, B. E. (2007a). Phosphoric acid fractionation factors for calcite and aragonite between 25 and 75°C: revisited. Chemical Geology 246, 135–146.
Phosphoric acid fractionation factors for calcite and aragonite between 25 and 75°C: revisited.Crossref | GoogleScholarGoogle Scholar |

Kim, S. T., O’Neil, J. R., Hillaire-Marcel, C., and Mucci, A. (2007b). Oxygen isotope fractionation between synthetic aragonite and water: influence of temperature and Mg2+ concentration. Geochimica et Cosmochimica Acta 71, 4704–4715.
Oxygen isotope fractionation between synthetic aragonite and water: influence of temperature and Mg2+ concentration.Crossref | GoogleScholarGoogle Scholar |

Kimirei, I. A., Nagelkerken, I., Trommelen, M., Blankers, P., van Hoytema, N., Hoeijmakers, D., Huijbers, C. M., Mgaya, Y. D., and Rypel, A. L. (2013a). What drives ontogenetic niche shifts of fishes in coral reef ecosystems? Ecosystems 16, 783–796.
What drives ontogenetic niche shifts of fishes in coral reef ecosystems?Crossref | GoogleScholarGoogle Scholar |

Kimirei, I. A., Nagelkerken, I., Mgaya, Y. D., and Huijbers, C. M. (2013b). The mangrove nursery paradigm revisited: otolith stable isotopes support nursery-to-reef movements by Indo-Pacific fishes. PLoS One 8, e66320.
The mangrove nursery paradigm revisited: otolith stable isotopes support nursery-to-reef movements by Indo-Pacific fishes.Crossref | GoogleScholarGoogle Scholar | 23776658PubMed |

Kitagawa, T., Ishimura, T., Uozato, R., Shirai, K., Amano, Y., Shinoda, A., Otake, T., Tsunogai, U., and Kimura, S. (2013). Otolith δ18O of Pacific bluefin tuna Thunnus orientalis as an indicator of ambient water temperature. Marine Ecology Progress Series 481, 199–209.
Otolith δ18O of Pacific bluefin tuna Thunnus orientalis as an indicator of ambient water temperature.Crossref | GoogleScholarGoogle Scholar |

Kok, P. H., Akhir, M. F., and Tangang, F. T. (2015). Thermal frontal zone along the east coast of Peninsular Malaysia. Continental Shelf Research 110, 1–15.
Thermal frontal zone along the east coast of Peninsular Malaysia.Crossref | GoogleScholarGoogle Scholar |

Kubota, K., Shirai, K., Murakami-Sugihara, N., Seike, K., Hori, M., and Tanabe, K. (2017). Annual shell growth pattern of the Stimpson’s hard clam Mercenaria stimpsoni as revealed by sclerochronological and oxygen stable isotope measurements. Palaeogeography, Palaeoclimatology, Palaeoecology 465, 307–315.
Annual shell growth pattern of the Stimpson’s hard clam Mercenaria stimpsoni as revealed by sclerochronological and oxygen stable isotope measurements.Crossref | GoogleScholarGoogle Scholar |

Le, D. Q., Tanaka, K., Hii, Y. S., Sano, Y., Nanjo, K., and Shirai, K. (2018). Importance of seagrass–mangrove continuum as feeding grounds for juvenile pink ear emperor Lethrinus lentjan in Setiu Lagoon, Malaysia: stable isotope approach. Journal of Sea Research 135, 1–10.
Importance of seagrass–mangrove continuum as feeding grounds for juvenile pink ear emperor Lethrinus lentjan in Setiu Lagoon, Malaysia: stable isotope approach.Crossref | GoogleScholarGoogle Scholar |

Lugendo, B. R., Pronker, A., Cornelissen, I., de Groene, A., Nagelkerken, I., Dorenbosch, M., van der Velde, G., and Yunus, D. M. (2005). Habitat utilisation by juveniles of commercially important fish species in a marine embayment in Zanzibar, Tanzania. Aquatic Living Resources 18, 149–158.
Habitat utilisation by juveniles of commercially important fish species in a marine embayment in Zanzibar, Tanzania.Crossref | GoogleScholarGoogle Scholar |

Luo, J., Serafy, J. E., Sponaugle, S., Teare, P. B., and Kieckbusch, D. (2009). Diel and seasonal movement of gray snapper (Lutjanus griseus) among subtropical seagrass, mangrove and coral reef habitats. Marine Ecology Progress Series 380, 255–269.
Diel and seasonal movement of gray snapper (Lutjanus griseus) among subtropical seagrass, mangrove and coral reef habitats.Crossref | GoogleScholarGoogle Scholar |

Mateo, I., Durbin, E. G., Appeldoorn, R. S., Adams, A. J., Juanes, F., Kingsley, R., Swart, P., and Durant, D. (2010). Role of mangroves as nurseries for French grunt Haemulon flavolinatum and schoolmaster Lutjanus apodus assessed by otolith elemental fingerprints. Marine Ecology Progress Series 402, 197–212.
Role of mangroves as nurseries for French grunt Haemulon flavolinatum and schoolmaster Lutjanus apodus assessed by otolith elemental fingerprints.Crossref | GoogleScholarGoogle Scholar |

McConnell, M. C., Thunell, R. C., Lorenzoni, L., Astor, Y., Wright, J. D., and Fairbanks, R. (2009). Seasonal variability in the salinity and oxygen isotopic composition of seawater from the Cariaco Basin, Venezuela: implications for paleosalinity reconstructions. Geochemistry Geophysics Geosystems 10, Q06019.
Seasonal variability in the salinity and oxygen isotopic composition of seawater from the Cariaco Basin, Venezuela: implications for paleosalinity reconstructions.Crossref | GoogleScholarGoogle Scholar |

McMahon, K. W., Fogel, M. L., Johnson, B. J., Houghton, L. A., and Thorrold, S. R. (2011). A new method to reconstruct fish diet and movement patterns from δ13C values in otolith amino acids. Canadian Journal of Fisheries and Aquatic Sciences 68, 1330–1340.
A new method to reconstruct fish diet and movement patterns from δ13C values in otolith amino acids.Crossref | GoogleScholarGoogle Scholar |

Mulcahy, S. A., Killingley, J. S., Phleger, C. F., and Berger, W. H. (1979). Isotopic composition of otoliths from a benthopelagic fish, Coryphaenoides acrolepis, Macrouridae: Gadiformes. Oceanologica Acta 2, 423–427.

Mumby, P. J. (2006). Connectivity of reef fish between mangroves and coral reefs: algorithms for the design of marine reserves at seascape scales. Biological Conservation 128, 215–222.
Connectivity of reef fish between mangroves and coral reefs: algorithms for the design of marine reserves at seascape scales.Crossref | GoogleScholarGoogle Scholar |

Nagelkerken, I., Roberts, C. M., van der Velde, G., Dorenbosch, M., van Riel, M. C., de la Morinere, E. C., and Nienhuis, P. H. (2002). How important are mangroves and seagrass beds for coral-reef fish? The nursery hypothesis tested on an island scale. Marine Ecology Progress Series 244, 299–305.
How important are mangroves and seagrass beds for coral-reef fish? The nursery hypothesis tested on an island scale.Crossref | GoogleScholarGoogle Scholar |

Nakamura, Y., Horinouchi, M., Shibuno, T., Tanaka, Y., Miyajima, T., Koike, I., Kurokura, H., and Sano, M. (2008). Evidence of ontogenetic migration from mangroves to coral reefs by black-tail snapper Lutjanus fulvus: stable isotope approach. Marine Ecology Progress Series 355, 257–266.
Evidence of ontogenetic migration from mangroves to coral reefs by black-tail snapper Lutjanus fulvus: stable isotope approach.Crossref | GoogleScholarGoogle Scholar |

Nelson, J., Hanson, C. W., Koenig, C., and Chanton, J. (2011). Influence of diet on stable carbon isotope composition in otoliths of juvenile red drum Sciaenops ocellatus. Aquatic Biology 13, 89–95.
Influence of diet on stable carbon isotope composition in otoliths of juvenile red drum Sciaenops ocellatus.Crossref | GoogleScholarGoogle Scholar |

Post, D. M. (2002). Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83, 703–718.
Using stable isotopes to estimate trophic position: models, methods, and assumptions.Crossref | GoogleScholarGoogle Scholar |

Pruell, R. J., Taplin, B. K., and Karr, J. D. (2010). Stable carbon and oxygen isotope ratios of otoliths differentiate juvenile winter flounder (Pseudopleuronectes americanus) habitats. Marine and Freshwater Research 61, 34–41.
Stable carbon and oxygen isotope ratios of otoliths differentiate juvenile winter flounder (Pseudopleuronectes americanus) habitats.Crossref | GoogleScholarGoogle Scholar |

Qu, T., Du, Y., Strachan, J., Meyers, G., and Slingo, J. (2005). Sea surface temperature and its variability in the Indonesian region. Journal of Oceanography 18, 50–61.
Sea surface temperature and its variability in the Indonesian region.Crossref | GoogleScholarGoogle Scholar |

Radtke, R. L., Showers, W., Moksness, E., and Lenz, P. (1996). Environmental information stored in otoliths: insights from stable isotopes. Marine Biology 127, 161–170.
Environmental information stored in otoliths: insights from stable isotopes.Crossref | GoogleScholarGoogle Scholar |

Reis-Santos, P., Tanner, S. E., Franca, S., Vasconcelos, R. P., Gillanders, B. M., and Cabral, H. N. (2015). Connectivity within estuaries: an otolith chemistry and muscle stable isotope approach. Ocean and Coastal Management 118, 51–59.
Connectivity within estuaries: an otolith chemistry and muscle stable isotope approach.Crossref | GoogleScholarGoogle Scholar |

Rilov, G., and Benayahu, Y. (2000). Fish assemblage on natural versus vertical artificial reefs: the rehabilitation perspective. Marine Biology 136, 931–942.
Fish assemblage on natural versus vertical artificial reefs: the rehabilitation perspective.Crossref | GoogleScholarGoogle Scholar |

Rioja-Nieto, R., and Alvarez-Filip, L. (2019). Coral reef systems of the Mexican Caribbean: status, recent trends and conservation. Marine Pollution Bulletin 140, 616–625.
Coral reef systems of the Mexican Caribbean: status, recent trends and conservation.Crossref | GoogleScholarGoogle Scholar | 30005908PubMed |

Rohling, E. J. (2013). Oxygen isotope composition of seawater. In ‘The Encyclopedia of Quaternary Science, Vol. 2’. (Ed. S. A. Elias.) pp. 915–922. (Elsevier: Amsterdam, Netherlands.)

Sakamoto, T., Komatsu, K., Yoneda, M., Ishimura, T., Higuchi, T., Shirai, K., Kamimura, Y., Watanabe, C., and Kawabata, A. (2017). Temperature dependence of δ18O in otolith of juvenile Japanese sardine: laboratory rearing experiment with micro-scale analysis. Fisheries Research 194, 55–59.
Temperature dependence of δ18O in otolith of juvenile Japanese sardine: laboratory rearing experiment with micro-scale analysis.Crossref | GoogleScholarGoogle Scholar |

Schaffner, F. C., and Swart, P. K. (1991). Influence of diet and environmental water on the carbon and oxygen stable isotopic signatures of seabird eggshell carbonate. Bulletin of Marine Science 48, 23–38.

Schwarcz, H. P., Gao, Y., Campana, S., Browne, D., Knyf, M., and Brand, U. (1998). Stable carbon isotope variations in otoliths of Atlantic cod (Gadus morhua). Canadian Journal of Fisheries and Aquatic Sciences 55, 1798–1806.
Stable carbon isotope variations in otoliths of Atlantic cod (Gadus morhua).Crossref | GoogleScholarGoogle Scholar |

Seaman, W. (2007). Artificial habitats and the restoration of degraded marine ecosystems and fisheries. Hydrobiology 580, 143–155.
Artificial habitats and the restoration of degraded marine ecosystems and fisheries.Crossref | GoogleScholarGoogle Scholar |

Serrano, X., Grosell, M., and Serafy, J. E. (2010). Salinity selection and preference of the grey snapper Lutjanus griseus: field and laboratory observations. Journal of Fish Biology 76, 1592–1608.
Salinity selection and preference of the grey snapper Lutjanus griseus: field and laboratory observations.Crossref | GoogleScholarGoogle Scholar | 20557618PubMed |

Shirai, K., Koyama, F., Murakami-Sugihara, N., Nanjo, K., Higuchi, T., Kohno, H., Watanabe, Y., Okamoto, K., and Sano, M. (2018). Reconstruction of the salinity history associated with movements of mangrove fishes using otolith oxygen isotopic analysis. Marine Ecology Progress Series 593, 127–139.
Reconstruction of the salinity history associated with movements of mangrove fishes using otolith oxygen isotopic analysis.Crossref | GoogleScholarGoogle Scholar |

Solomon, C. T., Weber, P. K., Cech, J. J., Ingram, B. L., Conrad, M. E., Machavaram, M. V., Pogodina, A. R., and Franklin, R. L. (2006). Experimental determination of the sources of otolith carbon and associated isotopic fractionation. Canadian Journal of Fisheries and Aquatic Sciences 63, 79–89.
Experimental determination of the sources of otolith carbon and associated isotopic fractionation.Crossref | GoogleScholarGoogle Scholar |

Suratman, S., Mohd Sailan, M. I., Hee, Y. Y., Bedurus, E. A., and Latif, M. T. (2015). A preliminary study of water quality index in Terengganu River Basin, Malaysia. Sains Malaysiana 44, 67–73.
A preliminary study of water quality index in Terengganu River Basin, Malaysia.Crossref | GoogleScholarGoogle Scholar |

Thomson, K. A., Ingraham, W. J., Healey, M. C., Leblond, P. H., Groot, C., and Healey, C. G. (1992). The influence of ocean currents on latitude of landfall and migration speed of sockeye salmon returning to the Fraser River. Fisheries Oceanography 1, 163–179.
The influence of ocean currents on latitude of landfall and migration speed of sockeye salmon returning to the Fraser River.Crossref | GoogleScholarGoogle Scholar |

Thorrold, S. R., Campana, S. E., Jones, C. M., and Swart, P. K. (1997). Factors determining 13C and 18O fractionation in aragonitic otoliths of marine fish. Geochimica et Cosmochimica Acta 61, 2909–2919.
Factors determining 13C and 18O fractionation in aragonitic otoliths of marine fish.Crossref | GoogleScholarGoogle Scholar |

Tieszen, L. L., Boutton, T. W., Tesdahl, K. G., and Slade, N. A. (1983). Fractionation and turnover of stable carbon isotopes in animal tissues: implications for δ13C analysis of diet. Oecologia 57, 32–37.
Fractionation and turnover of stable carbon isotopes in animal tissues: implications for δ13C analysis of diet.Crossref | GoogleScholarGoogle Scholar | 28310153PubMed |

Tohse, H., and Mugiya, Y. (2008). Sources of otolith carbonate: experimental determination of carbon incorporation rates from water and metabolic CO2, and their diel variations. Aquatic Biology 1, 259–268.
Sources of otolith carbonate: experimental determination of carbon incorporation rates from water and metabolic CO2, and their diel variations.Crossref | GoogleScholarGoogle Scholar |

Toor, H. S. (1964). Biology and fishery of the pig-face bream, Lethrinus lentjan Lacepede from Indian waters. III. Age and growth Indian Journal of Fisheries 11A, 597–620.

Trueman, C. N., Chung, M.-T., and Shores, D. (2016). Ecogeochemistry potential in deep time biodiversity illustrated using a modern deep-water case study. Philosophical Transactions of the Royal Society of London – B. Biological Sciences 371, 20150223.
Ecogeochemistry potential in deep time biodiversity illustrated using a modern deep-water case study.Crossref | GoogleScholarGoogle Scholar | 26977063PubMed |

Vaslet, A., France, C., Phillips, D. L., Feller, I. C., and Baldwin, C. C. (2011). Stable-isotope analyses reveal the importance of seagrass beds as feeding areas for juveniles of the speckled worm eel Myrophis punctatus (Teleostei: Ophichthidae) in Florida. Journal of Fish Biology 79, 692–706.
Stable-isotope analyses reveal the importance of seagrass beds as feeding areas for juveniles of the speckled worm eel Myrophis punctatus (Teleostei: Ophichthidae) in Florida.Crossref | GoogleScholarGoogle Scholar | 21884107PubMed |

Weidman, C., and Millner, R. (2000). High-resolution stable isotope records from North Atlantic cod. Fisheries Research 46, 327–342.
High-resolution stable isotope records from North Atlantic cod.Crossref | GoogleScholarGoogle Scholar |

Werner, E. E., and Gilliam, J. F. (1984). The ontogenetic niche and species interactions in size-structured populations. Annual Review of Ecology and Systematics 15, 393–425.
The ontogenetic niche and species interactions in size-structured populations.Crossref | GoogleScholarGoogle Scholar |

Xia, B., Gao, Q. F., Dong, S. L., and Wang, F. (2013). Carbon stable isotope turnover and fractionation in grass carp Ctenopharyngodon idella tissues. Aquatic Biology 19, 207–216.
Carbon stable isotope turnover and fractionation in grass carp Ctenopharyngodon idella tissues.Crossref | GoogleScholarGoogle Scholar |