Abstract
Diet is fundamental to an individual’s biology because energy acquired from food constrains growth and reproduction, which subsequently influences survival. It is, therefore, important to have a strong understanding of a population’s diet for species of conservation concern, such as the green turtle (Chelonia mydas). While the diet of adult green turtles is generally characterised as primarily herbivorous, growing evidence suggests variation in diet between and within populations is prevalent. We use complementary stable isotope analysis techniques to elucidate diet variation within a C. mydas population (ranging from small juveniles to adults) foraging at Ningaloo Reef in Western Australia. Analyses of multiple tissues and samples from ten individuals recaptured between 4 months and 4.5 years apart revealed that adults showed the highest levels of individual specialisation and consistency in diet over time. Analysis of red blood cell δ13C and δ15N values revealed macroalgae is likely the dominant food source for all size classes, and sub-adult and adults also ate animals (probably jellyfish). Compound-specific stable isotope analysis of amino acids indicated the main sources of essential amino acids for Ningaloo C. mydas were macroalgae or bacteria. Taken together, these results suggest C. mydas at Ningaloo conform to the general description of adult C. mydas diet as predominantly herbivorous, but diet varies with size and between adult individuals. Consideration of within-population diet variation will be important for predicting responses to stressors such as climate change, that directly affect foraging resources, as fitness consequences may vary for individuals with different diets.
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References
Amorocho DF, Reina RD (2007) Feeding ecology of the East Pacific green sea turtle Chelonia mydas agassizii at Gorgona National Park, Colombia. Endanger Species Res 3:43–51
Araújo MS, Bolnick DI, Layman CA (2011) The ecological causes of individual specialisation. Ecol Lett 14:948–958
Arthur KE, Balazs GH (2008) A comparison of immature green turtle (Chelonia mydas) diets among seven sites in the main Hawaiian Islands. Pac Sci 62:205–217
Arthur KE, Boyle MC, Limpus CJ (2008) Ontogenetic changes in diet and habitat use in green sea turtle (Chelonia mydas) life history. Mar Ecol Prog Ser 362:303–311
Arthur KE, McMahon KM, Limpus CJ, Dennison WC (2009) Feeding ecology of green turtles (Chelonia mydas) from Shoalwater Bay, Australia. Mar Turt Newsl 123:6–12
Arthur KE, Kelez S, Larsen T, Choy CA, Popp BN (2014) Tracing the biosynthetic source of essential amino acids in marine turtles using δ13C fingerprints. Ecology 95:1285–1293
Balazs GH, Chaloupka M (2004) Spatial and temporal variability in somatic growth of green sea turtles (Chelonia mydas) resident in the Hawaiian Archipelago. Mar Biol 145:1043–1059
Balazs GH (1980) Synopsis of biological data on the green turtle in the Hawaiian Islands. NOAA-TM-NMFS-SWFC-7, National Marine Fisheries Services, Honollulu
Bearhop S, Waldron S, Votier SC, Furness RW (2002) Factors that influence assimilation rates and fractionation of nitrogen and carbon stable isotopes in avian blood and feathers. Physiol Biochem Zool 75:451
Bearhop S, Adams CE, Waldron S, Fuller RA, MacLeod H (2004) Determining trophic niche width: a novel approach using stable isotope analysis. J Anim Ecol 73:1007–1012
Bjorndal KA (1979) Cellulose digestion and volatile fatty acid production in the green turtle Chelonia mydas. Comp Biochem Physiol 63:127
Bjorndal KA (1985) Nutritional ecology of sea turtles. Copeia 1985:736–751
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
Bjorndal KA, Suganuma H, Bolten AB (1991) Digestive fermentation in green turtles, Chelonia mydas, feeding on algae. Bull Mar Sci 48:166–171
Blasi MF, Tomassini L, Gelippi M, Careddu G, Insacco G, Polunin NVC (2018) Assessing resource use patterns of Mediterranean loggerhead sea turtles Caretta caretta (Linnaeus, 1758) through stable isotope analysis. Eur Zool J 85:71–87
Bolnick DI, Yang LH, Fordyce JA, Davis JM, Svanbäck R (2002) Measuring individual-level resource specialization. Ecology 83:2936–2941
Bolnick DI, Svanbӓck R, Fordyce JA, Yang LH, Davis JM, Hulsey CD, Forister ML (2003) The ecology of individuals: incidence and implications of individual specialization. Am Nat 161:1–28
Bolnick DI, Amarasekare P, Araújo MS, Bürger R, Levine JM, Novak M, Rudolf VHW, Schreiber SJ, Urban MC, Vasseur DA (2011) Why intraspecific trait variation matters in community ecology. Trends Ecol Evol 26:183–192
Bolten AB (2003) Variation in sea turtle life history patterns: neritic vs. oceanic developmental stages. In: Lutz PL, Musick JA, Wyneken J (eds) The biology of sea turtles. CRC Press, Boca Raton
Bond AL, Jardine TD, Hobson KA (2016) Multi-tissue stable-isotope analyses can identify dietary specialization. Methods Ecol Evol 7:1428–1437
Brand WA, Tegtmeyer AR, Hilkert A (1994) Compound-specific isotope analysis: extending toward 15N14N and 18O16O. Org Geochem 21:585–594
Brand-Gardner SJ, Limpus CJ, Lanyon JM (1999) Diet selection by immature green turtles, Chelonia mydas, in subtropical Moreton Bay, south-east Queensland. Aust J Zool 47:181–191
Bresette MJ, Witherington BE, Herren RM, Bagley DA, Gorham JC, Traxler SL, Crady CK, Hardy R (2010) Size-class partitioning and herding in a foraging group of green turtles Chelonia mydas. Endanger Species Res 9:105–116
Burgett CM, Burkholder DA, Coates KA, Fourqurean VL, Kenworthy WJ, Manuel SA, Outerbridge ME, Fourqurean JW (2018) Ontogenetic diet shifts of green sea turtles (Chelonia mydas) in a mid-ocean developmental habitat. Mar Biol 165:33
Burkholder DA, Heithaus MR, Thomson JA, Fourqurean JW (2011) Diversity in trophic interactions of green sea turtles Chelonia mydas on a relatively pristine coastal foraging ground. Mar Ecol Prog Ser 439:277–293
Campos P, Cardona L (2019) Individual variability in the settlement of juvenile green turtles in the western South Atlantic Ocean: relevance of currents and somatic growth rate. Mar Ecol Prog Ser 614:173–182
Cardona L, Aguilar A, Pazos L (2009) Delayed ontogenic dietary shift and high levels of omnivory in green turtles (Chelonia mydas) from the NW coast of Africa. Mar Biol 156:1487–1495
Cardona L, Campos P, Levy Y, Demetropoulos A, Margaritoulis D (2010) Asynchrony between dietary and nutritional shifts during the ontogeny of green turtles (Chelonia mydas) in the Mediterranean. J Exp Mar Biol Ecol 393:83–89
Cardona L, Martins S, Uterga R, Marco A (2017) Individual specialization and behavioral plasticity in a long-lived marine predator. J Exp Mar Biol Ecol 497:127–133
Cassata L, Collins LB (2008) Coral reef communities, habitats, and substrates in and near sanctuary zones of Ningaloo Marine Park. J Coast Res 24:139–151
Caut S, Angulo E, Courchamp F (2009) Variation in discrimination factors (∆15N and ∆13C): the effect of diet isotopic values and applications for diet reconstruction. J Appl Ecol 46:443–453
Cavallo C, Chiaradia A, Deagle BE, McInnes JC, Sánchez S, Hays GC, Reina RD (2018) Molecular analysis of predator scats reveals role of salps in temperature inshore food webs. Front Mar Sci 5:381
Ceriani SA, Roth JD, Tucker AD, Evans DR, Addison DS, Sasso CR, Ehrhart LM, Weishampel JF (2015) Carry-over effects and foraging ground dynamics of a major loggerhead breeding aggregation. Mar Biol 162:1955–1968
Chikaraishi Y, Ogawa NO, Kashiyama Y, Takano Y, Suga H, Tomitani A, Miyashita H, Kitazato H, Ohkouchi N (2009) Determination of aquatic food-web structure based on compound-specific nitrogen isotopic composition of amino acids. Limnol Oceanogr Methods 7:740–750
Chikaraishi Y, Steffan SA, Takano Y, Ohkouchi N (2015) Diet quality influences isotopic discrimination among amino acids in an aquatic vertebrate. Ecol Evol 5:2048–2059
Congdon JD, Dunham AE, Tinkle DW (1982) Energy budgets and life histories of reptiles. In: Gans C, Pough FH (eds) Biology of the reptilia. Academic Press, New York
Connolly RM, Guest MA, Melville AJ, Oakes JM (2004) Sulphur stable isotopes separate producers in marine food-web analysis. Oecologia 138:161–167
Dalerum F, Angerbjörn A (2005) Resolving temporal variation in vertebrate diets using naturally occurring stable isotopes. Oecologia 144:647–658
DeNiro MJ, Epstein S (1978) Influence of diet on the distribution of carbon isotopes in animals. Geochim Cosmochim Acta 42:495–506
DeNiro MJ, Epstein S (1981) Influence of diet on the distribution of nitrogen isotopes in animals. Geochim Cosmochim Acta 45:341–351
Dunham AE, Grant BW, Overall KL (1989) Interfaces between biophysical and physiological ecology and the population ecology of terrestrial vertebrate ectotherms. Physiol Zool 62:335–355
Eckert SA, Moore JE, Dunn DC, van Buiten RS, Eckert KL, Halpin PN (2008) Modelling loggerhead turtle movement in the Mediterranean: importance of body size and oceanography. Ecol Appl 18:290–308
Esteban N, Mortimer JA, Stokes HJ, Laloë J-O, Unsworth RKF, Hays GC (2020) A global review of green turtle diet: sea surface temperature as a potential driver of omnivory levels. Mar Biol 167:183
Ferreira RL, Ceia FR, Borges TC, Ramos JA, Bolten AB (2018) Foraging niche segregation between juvenile and adult hawksbill turtles (Eretmochelys imbricata) at Príncipe island, West Africa. J Exp Mar Biol Ecol 498:1–7
Figgener C, Bernardo J, Plotkin PT (2019) Beyond trophic morphology: stable isotopes reveal ubiquitous versatility in marine turtle trophic ecology. Biol Rev 94:1947–1973
Fry B (2006) Stable isotope ecology. Springer, New York
Fry B, Scalan RS, Winters JK, Parker PL (1982) Sulphur uptake by salt grasses, mangroves, and seagrasses in anaerobic sediments. Geochim Cosmochim Acta 46:1121–1124
Fuentes MMPB, Lawler IR, Gyuris E (2006) Dietary preferences of juvenile green turtles (Chelonia mydas) on a tropical reef flat. Wildl Res 33:671–678
Fukuoka T, Narazaki T, Kinoshita C, Sato K (2019) Diverse foraging habits of juvenile green turtles (Chelonia mydas) in a summer-restricted foraging habitat in the northwest Pacific Ocean. Mar Biol 166:25
Fulton CJ, Depczynski M, Holmes TH, Noble MM, Radford B, Wernberg T, Wilson SK (2014) Sea temperature shapes seasonal fluctuations in seaweed biomass within the Ningaloo coral reef ecosystem. Limnol Oceanogr 59:156–166
Gama LR, Domit C, Broadhurst MK, Fuentes M, Millar RB (2016) Green turtle Chelonia mydas foraging ecology at 25°S in the western Atlantic: evidence to support a feeding model driven by intrinsic and extrinsic variability. Mar Ecol Prog Ser 542:209–219
Garnett ST, Price IR, Scott FJ (1985) The diet of the green turtle, Chelonia mydas (L.), in Torres Strait. Wildl Res 12:103–112
Gillis AJ, Ceriani SA, Seminoff JA, Fuentes M (2018) Foraging ecology and diet selection of juvenile green turtles in the Bahamas: insights from stable isotope analysis and prey mapping. Mar Ecol Prog Ser 599:225–238
González Carman V, Botto F, Gaitán E, Albareda D, Campagna C, Mianzan H (2014) A jellyfish diet for the herbivorous green turtle Chelonia mydas in the temperate SW Atlantic. Mar Biol 161:339–349
Goodman Hall A, Avens L, McNeill JB, Wallace B, Goshe LR (2015) Inferring long-term foraging trends of individual juvenile loggerhead sea turtles using stable isotopes. Mar Ecol Prog Ser 537:265–276
Hancock JM, Vieira S, Jimenez V, Carvalho Rio J, Rebelo R (2018) Stable isotopes reveal dietary differences and site fidelity in juvenile green turtles foraging around São Tomé Island, West Central Africa. Mar Ecol Prog Ser 600:165–177
Harrison PM, Gutowsky LFG, Martins EG, Ward TD, Patterson DA, Cooke J, Power M (2017) Individual isotopic specializations predict subsequent inter-individual variation in movement in a freshwater fish. Ecology 98:608–615
Hatase H, Takai N, Matsuzawa Y, Sakamoto W, Omuta K, Goto K, Arai N, Fujiwara T (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
Hatase H, Sato K, Yamaguchi M, Takahashi K, Tsukamoto K (2006) Individual variation in feeding habitat use by adult female green sea turtles (Chelonia mydas): are they obligately neritic herbivores? Oecologia 149:52–64
Hays GC, Doyle TK, Houghton JDR (2018) A paradigm shift in the trophic importance of jellyfish? Trends Ecol Evol 33:874–884
Haywood JC, Fuller WJ, Godley BJ, Shutler JD, Widdicombe S, Broderick AC (2019) Global review and inventory: how stable isotopes are helping us understand ecology and inform conservation of marine turtles. Mar Ecol Prog Ser 613:217–245
Hazel J, Hamann M, Lawler IR (2013) Home range of immature green turtles tracked at an offshore tropical reef using automated passive acoustic technology. Mar Biol 160:617–627
Heaslip SG, Iverson SJ, Bowen WD, James MC (2012) Jellyfish support high energy intake of leatherback sea turtles (Dermochelys coriacea): video evidence from animal-borne cameras. PLoS ONE 7:e33259
Heithaus MR, McLash JJ, Frid A, Dill LM, Marshall GJ (2002) Novel insights into green sea turtle behaviour using animal-borne video cameras. J Mar Biol Assoc UK 82:1049–1050
Heithaus MR, Frid A, Wirsing AJ, Bejder L, Dill LM (2005) Biology of sea turtles under risk from tiger sharks at a foraging ground. Mar Ecol Prog Ser 288:285–294
Hemminga MA, Mateo MA (1996) Stable carbon isotopes in seagrasses: variability in ratios and use in ecological studies. Mar Ecol Prog Ser 140:285–298
Henschke N, Everett JD, Richardson AJ, Suthers IM (2016) Rethinking the role of salps in the ocean. Trends Ecol Evol 31:720–733
Hetherington ED, Seminoff JA, Dutton PH, Robison LC, Popp BN, Kurle CM (2018) Long-term trends in the foraging ecology and habitat use of an endangered species: an isotopic perspective. Oecologia 188:1273–1285
Hickey SM, Callow NJ, Phinn S, Lovelock CE, Duarte CM (2018) Spatial complexities in aboveground carbon stocks of a semi-arid mangrove community: a remote sensing height-biomass-carbon approach. Estuar Coast Shelf Sci 200:194–201
Hirth HF (1997) Synopsis of the biological data on the green turtle Chelonia mydas (Linnaeus 1758), U.S Fish and Wildlife Service Biological Report 97–1
Hobson KA, Clark RG (1992) Assessing avian diets using stable isotopes I: turnover of 13C in tissues. Condor 94:181–188
Hobson KA, Alisauskas RT, Clark RG (1993) Stable-nitrogen isotope enrichment in avian tissues due to fasting and nutritional stress: implications for isotopic analyses of diet. Condor 95:388–394
Howell LN, Reich KJ, Shaver DJ, Landry AM Jr, Gorga CC (2016) Ontogenetic shifts in diet and habitat of juvenile green sea turtles in the northwestern Gulf of Mexico. Mar Ecol Prog Ser 559:217–229
Howland MR, Corr LT, Young SMM, Jones V, Jim S, Van Der Merwe NJ, Mitchell AD, Evershed RP (2003) Expression of the dietary isotope signal in the compound-specific δ13C values of pig bone lipids and amino acids. Int J Osteoarchaeol 13:54–65
Ingram BA, Pitt KA, Barnes P (2017) Stable isotopes reveal a potential kleptoparasitic relationship between an ophiuroid (Ophiocnemis marmorata) and the semaeostome jellyfish, Aurelia aurita. J Plankton Res 39:138–146
Ingram BA (2015) The diversity and abundance of gelatinous zooplankton in north-western Australia and the association of Ophiocnemis marmorata (Echinodermata: Ophiuroidea) with Aurelia aurita (Cnidaria: Scyphozoa). Honours thesis, Griffith University
Ishikawa NF, Kato Y, Togashi H, Yoshimura M, Yoshimizu C, Okuda N, Tayasu I (2014) Stable nitrogen isotopic composition of amino acids reveals food web structure in stream ecosystems. Oecologia 175:911–922
IUCN (2019) The IUCN red list of threatened species. Version 2019–2 http://www.iucnredlist.org. Accessed 1 Dec 2019
Jackson AL, Inger R, Parnell AC, Bearhop S (2011) Comparing isotopic niche widths among and within communities: SIBER – Stable Isotope Bayesian Ellipses in R. J Anim Ecol 80:595–602
Johansson CL, Bellwood DR, Depczynski M (2010) Sea urchins, macroalgae and coral reef decline: a functional evaluation of an intact reef system, Ningaloo, Western Australia. Mar Ecol Prog Ser 414:65–74
Jones TT, Seminoff JA (2013) Feeding biology: advances from field-based observations, physiological studies, and molecular techniques. In: Wyneken J, Lohmann KJ, Musick JA (eds) The biology of sea turtles, vol 3. CRC Press, Boca Raton
Kobryn HT, Wouters K, Beckley LE, Heege T (2013) Ningaloo Reef: shallow marine habitats mapped using a hyperspectral sensor. PLoS ONE 8:e70105
Larsen T, Taylor DL, Leigh MB, O’Brien DM (2009) Stable isotope fingerprinting: a novel method for identifying plant, fungal, or bacterial origins of amino acids. Ecology 90:3526–3535
Larsen T, Wooller MJ, Fogel ML, O’Brien DM (2012) Can amino acid carbon isotope ratios distinguish primary producers in a mangrove ecosystem? Rapid Commun Mass Spectrom 26:1541–1548
Larsen T, Ventura M, Andersen N, O’Brien DM, Piatkowski U, McCarthy MD (2013) Tracing carbon sources through aquatic and terrestrial food webs using amino acid stable isotope fingerprinting. PLoS ONE 8:e73441
Layman CA, Araújo MS, Boucek R, Hammerschlag-Peyer CM, Harrison E, Jud ZR, Matich P, Rosenblatt AE, Vaudo JJ, Yeager LA, Post DM, Bearhop S (2012) Applying stable isotopes to examine food-web structure: an overview of analytical tools. Biol Rev 87:545–562
Lemons G, Lewison R, Komoroske L, Gaos A, Lai C-T, 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
Lemons GW, Lewison RL, Seminoff JA, Coppenrath CM, Popp BN (2020) Nitrogen isotope fractionation of amino acids from a controlled study on the green turtle (Chelonia mydas): expanding beyond Glx/Phe for trophic position. Mar Biol 167:1–13
Limpus C (2008) A biological review of Australian marine turtles. 2. Green turtle, Chelonia mydas (Linnaeus). Brisbane, Queensland Environmental Protection Agency
Limpus CJ, Limpus DJ (2000) Mangroves in the diet of Chelonia mydas in Queensland, Australia. Mar Turt Newsl 89:13–15
Limpus CJ, Walter DG (1980) The growth of immature green turtles (Chelonia mydas) under natural conditions. Herpetologica 36:162–165
Limpus CJ, Miller JD, Parmenter CJ, Limpus DJ (2003) The green turtle, Chelonia mydas, population of Raine Island and the northern Great Barrier Reef: 1843–2001. Memoir Qld Museum 49:349–440
Limpus CJ., Limpus DJ, Arthur KE, Parmenter CJ (2005) monitoring green turtle population dynamics in Shoalwater Bay: 2000–2004. Research publication No. 83, Great Barrier Reef Marine Park Authority Research Publication Series, Townsville
Makowski C, Seminoff JA, Salmon M (2006) Home range and habitat use of juvenile Atlantic green turtles (Chelonia mydas L.) on shallow reef habitats in Palm Beach, Florida, USA. Mar Biol 148:1167–1179
Marine Parks and Reserves Authority (2005) Management Plan for the Ningaloo Marine Park and Muiron Islands Marine Management Area 2005–2015: Management Plan No 52, Western Australia, Department of Conservation and Land Management
Martinez del Rio C, Sabat P, Anderson-Sprecher R, Gonzalez SP (2009) Dietary and isotopic specialization: the isotopic niche of three Cinclodes ovenbirds. Oecologia 161:149–159
Matich P, Heithaus MR, Layman CA (2011) Contrasting patterns of individual specialization and trophic coupling in two marine apex predators. J Anim Ecol 80:294–305
McCutchan JH, Lewis WM, Kendall C, McGrath CC (2003) Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos 102:378–390
McInnes JC, Alderman R, Lea M-A, Raymond B, Deagle BE, Phillips RA, Stanworth A, Thompson DR, Catry P, Weimerskirch H, Suazo CG, Gras M, Jarman SN (2017) High occurrence of jellyfish predation by black-browed and Campbell albatross identified by DNA metabarcoding. Mol Ecol 26:4831–4845
McMahon KW, McCarthy MD (2016) Embracing variability in amino acid δ15N fractionation: mechanisms, implications, and applications for trophic ecology. Ecosphere 7:e01511
McMahon KW, Newsome SD (2019) Amino acid isotope analysis: a new frontier in studies of animal migration and foraging ecology. In: Hobson KA, Wassenaar LI (eds) Tracking animal migration with stable isotopes. Elsevier, Amsterdam
McMahon KW, Fogel ML, Elsdon TS, Thorrold SR (2010) Carbon isotope fractionation of amino acids in fish muscle reflects biosynthesis and isotopic routing from dietary protein. J Anim Ecol 79:1132–1141
Minagawa M, Wada E (1984) Stepwise enrichment of 15N along food chains: further evidence and the relation between δ15N and animal age. Geochim Cosmochim Acta 48:1135–1140
Moncreiff CA, Sullivan MJ (2001) Trophic importance of epiphytic algae in subtropical seagrass beds: evidence from multiple stable isotope analyses. Mar Ecol Prog Ser 215:93–106
Morais RA, dos Santos RG, Longo GO, Yoshida ET, Stahelin GD, Horta PA (2014) Direct evidence for gradual ontogenetic dietary shift in the green turtle, Chelonia mydas. Chelonian Conserv Biol 13:260–266
Newsome SD, Martinez del Rio C, Bearhop S, Phillips DL (2007) A niche for isotopic ecology. Front Ecol Environ 5:429–436
Newsome SD, Clementz MT, Koch PL (2010) Using stable isotope biogeochemistry to study marine mammal ecology. Mar Mamm Sci 26:509–572
Nielsen JM, Popp BN, Winder M (2015) Meta-analysis of amino acid stable nitrogen isotope ratios for estimating trophic position in marine organisms. Oecologia 178:631–642
O’Connell TC (2017) ‘Trophic’ and ‘source’ amino acids in trophic estimation: a likely metabolic explanation. Oecologia 184:317–326
Ohkouchi N, Chikaraishi Y, Close HG, Fry B, Larsen T, Madigan DJ, McCarthy MD, McMahon KW, Nagata T, Naito YI, Ogawa NO, Popp BN, Steffan S, Takano Y, Tayasu I, Wyatt ASJ, Yamaguchi YT, Yokoyama Y (2017) Advances in the application of amino acid nitrogen isotopic analysis in ecological and biochemical studies. Org Geochem 113:150–174
Pajuelo M, Bjorndal KA, Arendt MD, Foley AM, Schroeder BA, Witherington BE, Bolten AB (2016) Long-term resource use and foraging specialization in male loggerhead turtles. Mar Biol 163:235
Patel SH, Panagopoulou A, Morreale SJ, Kilham SS, Karakassis I, Riggall T, Margaritoulis D, Spotila JR (2015) Differences in size and reproductive output of loggerhead turtles Caretta caretta nesting in the eastern Mediterranean Sea are linked to foraging site. Mar Ecol Prog Ser 535:231–241
Pearson RM, van de Merwe JP, Limpus CJ, Connolly RM (2017) Realignment of sea turtle isotope studies needed to match conservation priorities. Mar Ecol Prog Ser 583:259–271
Peavey LE, Popp BN, Pitman RL, Gaines SD, Arthur KE, Kelez S, Seminoff JA (2017) Opportunism on the high seas: foraging ecology of olive ridley turtles in the Eastern Pacific Ocean. Front Mar Sci 4:348
Pendoley K, Fitzpatrick J (1999) Browsing of mangroves by green turtles in Western Australia. Mar Turt Newsl 84:10
Peterson BJ, Fry B (1987) Stable isotopes in ecosystem studies. Annu Rev Ecol Syst 18:293–320
Phillips DL, Gregg JW (2003) Source partitioning using stable isotopes: coping with too many sources. Oecologia 136:261–269
Phillips DL, Inger R, Bearhop S, Jackson AL, Moore JW, Parnell AC, Semmens BX, Ward EJ (2014) Best practices for use of stable isotope mixing models in food-web studies. Can J Zool 92:823–835
Popp BN, Graham BS, Olson RJ, Hannides CCS, Lott MJ, López-Ibarra GA, Galván-Magaña F, Fry B (2007) Insight into the trophic ecology of yellowfin tuna, Thunnus albacares, from the compound-specific nitrogen isotope analysis of proteinaceous amino acids. In: Dawson T, Siegwolf R (eds) Stable isotopes as indicators of ecological change. Elsevier/Academic Press, Cambridge, pp 173–190
Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83:703–718
Preen AR, Marsh H, Lawler IR, Prince RIT, Shepherd R (1997) Distribution and abundance of dugongs, turtles, dolphins and other megafauna in Shark Bay, Ningaloo Reef and Exmouth Gulf, Western Australia. Wildl Res 24:185–208
Prince RI, Wann RH, Wann JP, Williams AA (2012) Species, size classes, and apparent growth rates of sea turtles recorded associating with a net and trap fishery in Exmouth Gulf, Western Australia: December 1990–June 1998. Mar Turt Newsl 134:3–8
Prior B, Booth DT, Limpus CJ (2016) Investigating diet and diet switching in green turtles (Chelonia mydas). Aust J Zool 63:365–375
R Development Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Ramirez MD, Besser AC, Newsome SD, McMahon KW (2021) Meta-analysis of primary producer amino acid δ15N values and their influence on trophic position estimates. Methods Ecol Evol 12:1750–1767
Reich KJ, Bjorndal KA, Bolten AB (2007) The ‘lost years’ of green turtles: using stable isotopes to study cryptic lifestages. Biol Let 3:712–714
Reich KJ, Bjorndal KA, Martínez del Rio C (2008) Effects of growth and tissue type on the kinetics of 13C and 15N incorporation in a rapidly growing ectotherm. Oecologia 155:651–663
Roughgarden J (1972) Evolution of niche width. Am Nat 106:683–718
Rubenstein DR, Hobson KA (2004) From birds to butterflies: animal movement patterns and stable isotopes. Trends Ecol Evol 19:256–263
Santos RG, Martins AS, Batista MB, Horta PA (2015) Regional and local factors determining green turtle Chelonia mydas foraging relationships with the environment. Mar Ecol Prog Ser 529:265–277
Seminoff JA, Jones TT, Eguchi T, Jones DR, Dutton PH (2006) Stable isotope discrimination (δ13C and δ15N) between soft tissues of the green sea turtle Chelonia mydas and its diet. Mar Ecol Prog Ser 308:271–278
Seminoff JA, Bjorndal KA, Bolten AB (2007) Stable carbon and nitrogen discrimination and turnover in pond sliders Trachemys scripta: insights for trophic study of freshwater turtles. Copeia 3:534–542
Seminoff JA, Benson SR, Arthur KE, Eguchi T, Dutton PH, Tapilatu RF, Popp BN (2012) Stable isotope tracking of endangered sea turtles: validation with satellite telemetry and δ15N analysis of amino acids. PLoS ONE 7:1–11
Silfer JA, Engel MH, Macko SA, Jumeau EJ (1991) Stable carbon isotope analysis of amino acid enantiomers by conventional isotope ratio mass spectrometry and combined gas chromatography/isotope ratio mass spectrometry. Anal Chem 63:370–374
Skrzypek G (2013) Normalization procedures and reference material selection in stable HCNOS isotope analyses: an overview. Anal Bioanal Chem 405:2815–2823
Skrzypek G, Paul D (2006) δ13C analyses of calcium carbonate: comparison between the GasBench and elemental analyzer techniques. Rapid Commun Mass Spectrom 20:2915–2920
Somes CJ, Schmittner A, Galbraith ED, Lehmann MF, Altabet MA, Montoya JP, Letelier RM, Mix AC, Bourbonnais A, Eby M (2010) Simulating the global distribution of nitrogen isotopes in the ocean. Glob Biogeochem Cycles 24:GB4019
Stock BC, Jackson AL, Ward EJ, Parnell AC, Phillips DL, Semmens BX (2018) Analyzing mixing systems using a new generation of Bayesian tracer mixing models. PeerJ 6:e5096
Stubbs JL, Marn N, Vanderklift MA, Fossette S, Mitchell N (2020) Simulated growth and reproduction of green turtles (C. mydas) under climate change and marine heatwave scenarios. Ecol Model 431:109185
Thiebot J-B, McInnes JC (2019) Why do marine endotherms eat gelatinous prey? ICES J Mar Sci 77:58–71
Thomson JA, Whitman ER, Garcia-Rojas MI, Bellgrove A, Ekins M, Hays GC, Heithaus MR (2018) Individual specialization in a migratory grazer reflects long-term diet selectivity on a foraging ground: implications for isotope-based tracking. Oecologia 188:429–439
Turner Tomaszewicz CN, Seminoff JA, Price M, Kurle CM (2017) Stable isotope discrimination factors and between-tissue isotope comparisons for bone and skin from captive and wild green sea turtles (Chelonia mydas). Rapid Commun Mass Spectrom 31:1903–1914
Vander Zanden HB, Bjorndal KA, Reich KJ, Bolten AB (2010) Individual specialists in a generalist population: results from a long-term stable isotope series. Biol Lett 6:711–714
Vander Zanden HB, Bjorndal KA, Mustin W, Ponciano JM, Bolten AB (2012) Inherent variation in stable isotope values and discrimination factors in two life stages of green turtles. Physiol Biochem Zool 85:431–441
Vander Zanden HB, Arthur KE, Bolten AB, Popp BN, Lagueux CJ, Harrison E, Campbell CL, Bjorndal KA (2013a) Trophic ecology of a green turtle breeding population. Mar Ecol Prog Ser 476:237–249
Vander Zanden HB, Bjorndal KA, Bolten AB (2013b) Temporal consistency and individual specialization in resource use by green turtles in successive life stages. Oecologia 173:767–777
Vander Zanden HB, Pfaller JB, Reich KJ, Pajuelo M, Bolten AB, Williams KL, Frick MG, Shamblin BM, Nairn CJ, Bjorndal KA (2014) Foraging areas differentially affect reproductive output and interpretation of trends in abundance of loggerhead turtles. Mar Biol 161:585–598
Vanderklift MA, Bearham D (2014) Variation in δ13C and δ15N of kelp is explained by light and productivity. Mar Ecol Prog Ser 515:111–121
Vanderklift MA, Ponsard S (2003) Sources of variation in consumer-diet δ15N enrichment: a meta-analysis. Oecologia 136:169–182
Vanderklift MA, Babcock RC, Barnes PB, Cresswell AK, Feng M, Haywood MDE, Holmes TH, Lavery PS, Pillans RD, Smallwood CB, Thomson DP, Tucker AP, Waples K, Wilson SK (2020a) The oceanography and marine ecology of Ningaloo, a World Heritage Area. Oceanogr Mar Biol Annu Rev 58:143–178
Vanderklift MA, Pillans RD, Robson NA, Skrzypek G, Stubbs JL, Tucker AD (2020b) Comparisons of stable isotope composition among tissues of green turtles. Rapid Commun Mass Spectrom 34:e8839
Venables WN, Ripley BD (2002) Modern applied statistics with S. Springer, New York
Wallace BP, Kilham SS, Paladino FV, Spotila JR (2006) Energy budget calculations indicate resource limitation in Eastern Pacific leatherback turtles. Mar Ecol Prog Ser 318:263–270
Wiley AE, Rossman A, Ostrom PH, France CAM, Penniman J, Bailey C, Duvall F, Zipkin EF, James HF (2019) From ecologically equivalent individuals to contrasting colonies: quantifying isotopic niche and individual foraging specialization in an endangered oceanic seabird. Mar Biol 166:39
Williams NC, Bjorndal KA, Lamont MM, Carthy RR (2014) Winter diets of immature green turtles (Chelonia mydas) on a northern feeding ground: integrating stomach contents and stable isotope analyses. Estuaries Coasts 37:986–994
Williard AS, Hall AG, Fujisaki I, McNeill JB (2017) Oceanic overwintering in juvenile green turtles Chelonia mydas from a temperate latitude foraging ground. Mar Ecol Prog Ser 564:235–240
Wolf N, Carleton SA, Martínez del Rio C (2009) Ten years of experimental animal isotopic ecology. Funct Ecol 23:17–26
Wood Jr JR (1974) Amino-acids essential for the growth of young green sea turtles (Chelonia mydas). In: Proceedings of the annual meeting. World Mariculture Society, 1974. Wiley Online Library, p 233–248
Acknowledgements
We thank Doug Ford and Grzegorz Skrzypek at the West Australian Biogeochemistry Centre (WABC) for measuring bulk tissue isotope ratios and we thank Mina Brock for assistance in preparing samples for AA-CSIA. We thank the many volunteers and CSIRO staff that assisted in the field sampling turtles. In addition, we thank Norman Lai and Natalie Robson for assistance in sample preparation.
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This study was supported by the BHP-CSIRO Ningaloo Outlook Marine Research Partnership. JS was supported by an Australian Government Research Training Program Scholarship and BHP Marine Research Scholarship at The University of Western Australia.
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JS and MV conceptualised the study. JS, MV, and RP collected the samples; JS, MV, and AR performed the laboratory work. JS performed the statistical analyses, JS wrote the manuscript with contributions from all the authors. All the authors reviewed, edited, and approved the article.
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This research was conducted under WA Department of Biodiversity Conservation and Attractions (DBCA) permits (SF008922, SF009590, SF010221, SF010794, 08-000539-2, 08-000539-3, SW016071), Department of Primary Industries and Regional Development exemptions (3141, 3218), and CSIRO Ecosystem Science animal ethics committee approval 2014-07.
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Stubbs, J.L., Revill, A.T., Pillans, R.D. et al. Stable isotope composition of multiple tissues and individual amino acids reveals dietary variation among life stages in green turtles (Chelonia mydas) at Ningaloo Reef. Mar Biol 169, 72 (2022). https://doi.org/10.1007/s00227-022-04055-6
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DOI: https://doi.org/10.1007/s00227-022-04055-6