Diverse foraging habits of juvenile green turtles (Chelonia mydas) in a summer-restricted foraging habitat in the northwest Pacific Ocean
Green turtles in year-round neritic foraging habitats are widely considered to have small home ranges and to mainly feed on plant-based diets. In contrast, few studies have examined the summer-restricted habitats to which these turtles seasonally migrate. In this study, we investigated the foraging habits of green turtles migrating to the Sanriku Coast, a summer-restricted foraging habitat in a temperate area (38–39°N) of the northwest Pacific Ocean, using stable isotope analysis and biologging experiments from 2007 to 2015. Stable isotope analysis (n = 40, straight carapace length (SCL): 36.8–90.9 cm) indicated that most of the turtles, especially all smaller turtles (n = 35, SCL < 58 cm), relied on gelatinous prey before arriving at the Sanriku Coast. According to the biologging experiments (451.2 h of behavioral data and 43.2 h of video data, n = 6, SCL: 44.5–81.0 cm), the turtles shifted their main food to macro-algae (135 out of 148 feeding events) and consumed it at the sea bottom during their stay in the specific localized area of the Sanriku Coast. However, the turtles still consumed gelatinous prey in midwater during their movement to other locations along the Sanriku Coast and/or during their migration to southern overwintering habitats (13 events). These results indicated that green turtles migrating to the Sanriku Coast exhibit dietary diversity relative to year-round habitats, and the turtles in this area seem to consume gelatinous prey during the transit period in addition to feeding on macro-algae during the resident period.
We are grateful to all volunteers from the Fisheries Cooperative Association of Funakoshi Bay, Hirota Bay, Kamaishi Bay, Kamaishi-Tobu, Michishita, Miyako, Ofunato, Okirai, Omoe, Shin-Otsuchi, Ryori, Sanriku-Yamada, Sasaki, Toni, Yamaichi, and Yoshihama, who provided us with wild-caught sea turtles. Special thanks to M. Kurosawa, K. Morita, J. Takada, M. Hirano, T. Abe, T. Tashiro, I. Okaya, K. Takahashi and T. Kikuchi, for their great assistance in retrieving the data loggers. We also thank Y. Fujiwara, S. Takuma, H. Murasaki, K. Onitsuka, I. Nakamura, N. Miyata, S. Nobata, M. Yamane, T. Iwata, H. Nishizawa, and T. Abe who assisted in the field. We appreciate T. Miyajima and N. Saotome for their support with the stable isotope analysis. This study was performed under the Cooperative Program of Atmosphere and Ocean Research Institute, The University of Tokyo. We acknowledge the use of the Maptool (http://www.seaturtle.org/maptool/) program for mapping the study site and data logger retrieved sites. We thank three anonymous reviewers for their constructive comments and recommendations. Finally, we would like to dedicate our work to all the people in our study area who were severely affected by the tsunami on 11 March 2011.
This study was financially supported by the Tohoku Ecosystem-Associated Marine Sciences (TEAMS), the Bio-Logging Science, the University of Tokyo (UTBLS), a Japanese Society for the Promotion of Science (JSPS) research Grant (24241001 to KS), a JSPS Research Fellowship for Young Scientists (16J06542 to TF).
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
This study was performed in accordance with the guidelines of the Animal Ethic Committee of the University of Tokyo, and the protocol of the study was approved by this committee (P12-13, P13-6, P14-3, and P15-7).
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- Bjorndal KA (1997) Foraging ecology and nutrition of sea turtles. In: Lutz PL, Musick JA (eds) The biology of sea turtles. CRC Press, Boca Raton, pp 237–283Google Scholar
- Epperly SP, Braun J, Veishlow A (1995) Sea turtles in North Carolina waters. Conserv Biol 9:384–394. https://doi.org/10.1046/j.1523-1739.1995.9020384.x CrossRefGoogle Scholar
- Fukuoka (2016) Foraging ecology of green sea turtles (Chelonia mydas) migrating to the northern Pacific coast of Japan. Ph.D. dissertation, University of Tokyo, Tokyo, Japan, pp 166Google Scholar
- González Carman V, Alvarez K, Prosdocimi L, Inchaurraga MC, Dellacasa RF, Faiella A, Echenique C, González R, Andrejuk J, Mianzan H, Campagna C, Albareda DA (2011) Argentinian coastal waters: a temperate habitat for three species of threatened sea turtles. Mar Biol Res 7:500–508. https://doi.org/10.1080/17451000.2010.528772 CrossRefGoogle Scholar
- Hatase H, Takai N, Matsuzawa Y et al (2002) Size-related differences in feeding habitat use of adult female loggerhead turtles Caretta caretta around Japan determined by stable isotope analyses and satellite telemetry. Mar Ecol Prog Ser 233:273–281. https://doi.org/10.3354/meps233273 CrossRefGoogle Scholar
- Hirth HF (1997) Synopsis of the biological data on the green turtle, Chelonia mydas (Linnaeus 1758). United States Fish and Wildlife Service Biological Report 97-1Google Scholar
- Ishihara T (2012) Life history. In: Kamezaki N (ed) Natural history of sea turtles in Japan. University of Tokyo Press, Tokyo, pp 57–83Google Scholar
- Kameda K, Ishihara T (2009) Gut contents analysis of green turtles (Chelonia mydas) in Japan. UMIGAME Newsl Jpn 81:17–23 (in Japanese with English abstract) Google Scholar
- Kameda K, Wakatsuki M, Kamezaki N (2013) Population structure and growth rate of the green turtle Chelonia mydas, on feeding grounds at Kuroshima Island, of Yaeyama group, Ryukyu Archipelago. Biol Mag Okinawa 51:93–100 (in Japanese with English abstract) Google Scholar
- King WF (1982) Historical review of the decline of the green turtle and the hawksbill. In: Bjorndal KA (ed) Biology and conservation of sea turtles. Smithsonian Institute Press, Washington DC, pp 183–188Google Scholar
- Lemons G, Lewison R, Komoroske L, Gaos A, Lai CT, Dutton P, Eguchi T, LeRoux R, Seminoff JA (2011) Trophic ecology of green sea turtles in a highly urbanized bay: insights from stable isotopes and mixing models. J Exp Mar Biol Ecol 405:25–32. https://doi.org/10.1016/j.jembe.2011.05.012 CrossRefGoogle Scholar
- Ministry of the Environment (2011) Marine biodiversity conservation strategy. Nature Conservation Bureau, Tokyo, p 51Google Scholar
- Mitani Y, Sato K, Ito S, Cameron MF, Siniff DB, Naito Y (2003) A method for reconstructing three-dimensional dive profiles of marine mammals using geomagnetic intensity data: results from two lactating Weddell seals. Polar Biol 26:311–317. https://doi.org/10.1007/s00300-003-0487-y CrossRefGoogle Scholar
- Musick JA, Limpus CJ (1997) Habitat utilization and migration in juvenile sea turtles. In: Lutz PL, Musick JA (eds) The biology of sea turtles. CRC Press, Boca Raton, pp 137–163Google Scholar
- Narazaki T, Shiomi K (2010) Reconstruction of 3-D path (ThreeD_path). http://japan-biologgingsci.org/home/macro/threed_path/. Accessed 08 July 2017
- Nature Conservation Bureau (1994) The report of the marine biotic environment survey in the 4th national survey on the natural environment, vol 2. In: Algal and sea-grass beds Tokyo, p 400 (in Japanese with English summary) Google Scholar
- Nishizawa H, Naito Y, Suganuma H, Abe O, Okuyama J, Hirate K, Tanaka S, Inoguchi E, Narushima K, Kobayashi K, Ishii H, Tanizaki S, Kobayashi M, Goto A, Arai N (2013) Composition of green turtle feeding aggregations along the Japanese archipelago: implications for changes in composition with current flow. Mar Biol 160:2671–2685. https://doi.org/10.1007/s00227-013-2261-1 CrossRefGoogle Scholar
- Nishizawa H, Narazaki T, Fukuoka T, Sato K, Hamabata T, Kinoshita M, Arai N (2014) Juvenile green turtles on the northern edge of their range: mtDNA evidence of long-distance westward dispersals in the northern Pacific Ocean. Endang Species Res 24:171–179. https://doi.org/10.3354/esr00592 CrossRefGoogle Scholar
- Odate K (1994) Zooplankton biomass and its long-term variation in the western North Pacific Ocean, Tohoku sea area, Japan. Bull Tohoku Natl Fish Res Inst 56:115–173 (in Japanese with English summary) Google Scholar
- Okamoto K, Ishihara T, Taniguchi M, Yamashita N, Kamezaki N (2011) Occurrence of the sea turtles at the coastal water of Kumanonada. Umigame Newsl Jpn 88:13–17 (in Japanese) Google Scholar
- Okuyama J, Nakajima K, Noda T, Kimura S, Kamihata H, Kobayashi M, Arai N, Kagawa S, Kawabata Y, Yamada H (2013) Ethogram of immature green turtles: behavioral strategies for somatic growth in large marine herbivores. PLoS One 8:e65783. https://doi.org/10.1371/journal.pone.0065783 CrossRefPubMedPubMedCentralGoogle Scholar
- Owens D, Ruiz GW (1980) New methods of obtaining blood and cerebrospinal fluid from marine turtles. Herpetologica 1:17–20Google Scholar
- Pritchard PCH (1997) Evolution, phylogeny, and current status in the biology of sea turtles. In: Lutz PL, Musick JA (eds) Biology of sea turtles. CRC, Boca Raton, pp 1–28Google Scholar
- R Core Team (2015) The R Foundation for Statistical Computing. https://www.r-project.org/. Accessed 05 Feb 2018
- Renaud ML, Carpenter JA, Williams JA (1995) Activities of juvenile green turtle, Chelonia mydas, at a jettied pass in South Texas. Fish Bull 93:586–593Google Scholar
- Sato K, Otsuki M, Morita K, Kurosawa M, Takada J (2007) Result of hydrographic and meteorologic observation in 2006. Annu Rep Int Coast Res Center Univ Tokyo 32:37–47 (in Japanese) Google Scholar
- Seminoff JA (2004) Chelonia mydas. The IUCN Red List of Threatened Species 2004: e.T4615A11037468 http://dx.doi.org/10.2305/IUCN.UK.2004.RLTS.T4615A11037468.en. Downloaded on 17 August 2017
- Seminoff JA, Allen CD, Balazs GH, et al (2015) Status review of the green turtle (Chelonia mydas) under the U.S. Endangered Species Act. NOAA Technical Memorandum NMFS, p 571Google Scholar
- Suganuma H (1994) Green sea turtle. In: Fisheries Agency (ed) Basic report of rare wild aquatic species of Japan, vol 1. Japan Fisheries Resource Conservation Association, Tokyo, pp 469–478Google Scholar
- Thomson JA, Cooper AB, Burkholder DA, Heithaus MR, Dill LM (2012) Heterogeneous patterns of availability for detection during visual surveys: spatiotemporal variation in sea turtle dive–surfacing behaviour on a feeding ground. Methods Ecol Evol 3:378–387. https://doi.org/10.1111/j.2041-210X.2011.00163.x CrossRefGoogle Scholar
- Wilson RP, Liebsch N, Davies IM, Quintana F, Weimerskirch H, Storch S, Lucke K, Siebert U, Zankl S, Müller G, Zimmer I, Scolaro A, Campagna C, Plotz J, Bornemann H, Teilmann J, McMahon CR (2007) All at sea with animal tracks; methodological and analytical solutions for the resolution of movement. Deep Sea Res II 54:193–210. https://doi.org/10.1016/j.dsr2.2006.11.017 CrossRefGoogle Scholar