Skip to main content

Evaluating different spatial scales of forage item availability to determine diet selection of juvenile green turtles (Chelonia mydas)

Abstract

Diet selection by a species is determined by comparing the consumption (i.e., use) and abundance (i.e., availability) of prey within their area of occupancy. Because individuals commonly use only a portion of habitat available to them (e.g., a 10-ha home range within a 1000-ha foraging habitat), it is important to quantify forage availability within individuals’ home ranges and core areas, and include these availabilities when calculating diet selection. However, studies of diet selection often consider prey availability across the entire foraging habitat of a species and not within individual home ranges/core areas. Here, we explore how spatial variability in prey availability may influence the results of diet selection for juvenile green turtles, Chelonia mydas, foraging in Bimini, Bahamas. Stable isotope analysis was used to determine prey use and satellite telemetry to infer movements and forage availability for each turtle. Forage availability was assessed at three spatial scales: (1) the full extent of the foraging area (2) across each respective individual’s 95% utilization distribution (UD), or home ranges, and (3) across each individual’s 50% UD, or core areas. Further, we compared potential differences in diet selection by using three selection indices (Ivlev’s, Johnson’s and Chesson’s). Diet selection results varied among individuals and were influenced by the spatial scale of forage items available and the index used. Diet selection variability was observed at various spatial scales and in all indices. Our results highlight the need for careful consideration of the diet selection index and the spatial scale at which prey/forage availability is considered when determining a species’ diet selection. Selecting a more sensitive index will help identify priority resources and/or habitats that are important to species, which in turn carries conservation and management implications.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Data/Code availability

Data and any available visuals (i.e., figure, table) will be provided upon reasonable request submitted to the corresponding author. Further, any codes created to assist in data analysis and/or any software application utilized in this current study can and will be provided upon reasonable request submitted to the corresponding author.

References

  1. Alldredge JR, Ratti JT (1986) Comparison of some statistical techniques for analysis of resource selection. J Wildl Manag 50:157–165. https://doi.org/10.2307/3801507

    Article  Google Scholar 

  2. Alldredge JR, Ratti JT (1992) Further comparison of some statistical techniques for analysis of resource selection. J Wildl Manage 56:1–9. https://doi.org/10.2307/3808785

    Article  Google Scholar 

  3. Bailey H, Shillinger G, Palacios D, Bograd S, Spotila J, Paladino F, Block B (2008) Identifying and comparing phases of movement by leatherback turtles using state-space models. J Exp Mar Bio Ecol 356:128–135. https://doi.org/10.1016/j.jembe.2007.12.020

    Article  Google Scholar 

  4. Bartonek JC, Hickey JJ (1969) Selective feeding by juvenile diving ducks in summer. Auk 86:443–457. https://doi.org/10.2307/4083407

    Article  Google Scholar 

  5. Benhamou S (2011) Dynamic approach to space and habitat use based on biased random bridges. PLoS ONE. https://doi.org/10.1371/journal.pone.0014592

    Article  PubMed  PubMed Central  Google Scholar 

  6. Bjorndal KA (1989) Flexibility of digestive responses in two gerenalist herbivores, the tortoises Geochelone carbonaria and Geochelone denticulata. Oecologia 78(3):317–321. https://doi.org/10.1007/BF00379104

    Article  PubMed  Google Scholar 

  7. Bjorndal KA (1997) Foraging ecology and nutrition of sea turtles. In: Lutz PL, Musick JA (eds) The biology of sea turtles, vol 1. pp 400–406. Boca Raton, FL, https://doi.org/10.1201/9780203737088

  8. Bolnick DI, Ingram T, Stutz WE, Snowberg LK, Lau OL, Pauli JS (2010) Ecological release from interspecific competition leads to decoupled changes in population and individual niche width. Proc R Soc B Biol Sci 277:1789–1797. https://doi.org/10.1098/rspb.2010.0018

    Article  Google Scholar 

  9. Bradshaw CJA, Hindell MA, Best NJ, Phillips KL, Wilson G, Nichols PD (2003) You are what you eat: describing the foraging ecology of southern elephant seals (Mirounga leonina) using blubber fatty acids. Proc R Soc B Biol Sci 270 (1521):1283–1292. https://doi.org/10.1098/rspb.2003.2371

    Article  Google Scholar 

  10. Boyd IL (1996) Temporal scales of foraging in a marine predator. Ecol 77:426–434. https://doi.org/10.1098/rspb.2003.2371

    Article  Google Scholar 

  11. Brown MBGJ, Gemmill CEC, Miller S, Wehi PM (2018) Diet selectivity in a terrestrial forest invertebrate, the Auckland tree wētā, across three habitat zones. Ecol Evol 8:2495–2503. https://doi.org/10.1002/ece3.3763

    Article  PubMed  PubMed Central  Google Scholar 

  12. Calenge C (2015a) Analysis of animal movements in R: the adehabitatLT package.

  13. Calenge C (2015b) Home range estimation in R : the adehabitatHR Package. R Vignette. https://doi.org/10.1111/j.1365-2656.2006.01186.x

    Article  Google Scholar 

  14. 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. https://doi.org/10.1007/s00227-009-1188-z

    CAS  Article  Google Scholar 

  15. Chesson J (1978) Measuring preference in selective predation. Ecology 59(2):211–215. https://doi.org/10.2307/1936364

    Article  Google Scholar 

  16. Chesson J (1983) The estimation and analysis of preference and its relationship to foraging models. Ecol 64:1297–1304. https://doi.org/10.2307/1937838

    Article  Google Scholar 

  17. Christianen MJA, Govers LL, Bouma TJ, Kiswara W, Roelofs JGM, Lamers LPM, van Katwijk MM (2012) Marine megaherbivore grazing may increase seagrass tolerance to high nutrient loads. J Ecol 100:546–560. https://doi.org/10.1111/j.1365-2745.2011.01900.x

    CAS  Article  Google Scholar 

  18. CLS (2011) Argos User's Manual. https://www.argos-system.org/files/pmedia/public/r363_9_argosmanual_en.pdf Accessed 16 May 2020

  19. Cock MJW (1978) The assessment of preference. J Anim Ecol 47:805–816. https://doi.org/10.2307/3672

    Article  Google Scholar 

  20. Dale JJ, Wallsgrove NJ, Popp BN, Holland KN (2011) Nursery habitat use and foraging ecology of the brown stingray Dasyatis lata determined from stomach contents, bulk and amino acid stable isotopes. Mar Ecol Prog Ser 433:221–236. https://doi.org/10.3354/meps09171

    Article  Google Scholar 

  21. Falkenhaug T, Dalpadado P (2014) Diet composition and food selectivity of sprat (Sprattus sprattus) in Hardangerfjord, Norway. Mar Biol Res 10:203–215. https://doi.org/10.1080/17451000.2013.810752

    Article  Google Scholar 

  22. Fieberg J, Borger L (2012) Could you please phrase “home range” as a question? J Mammal 93(4):890–902. https://doi.org/10.1644/11-MAMM-S-172.1

    Article  Google Scholar 

  23. Ford RG (1983) Home range in a patchy environment : optimal foraging predictions. Am Zool 23:315–326. https://doi.org/10.1093/icb/23.2.315

    Article  Google Scholar 

  24. Forsyth DM, Coomes DA, Hall GMJ, Nugent G (2002) Diet and diet preferences of introduced ungulates (Order: Artiodactyla) in New Zealand. NZ J Zool 29:323–343. https://doi.org/10.1080/03014223.2002.9518316

    Article  Google Scholar 

  25. 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. https://doi.org/10.1071/WR05081

    Article  Google Scholar 

  26. Fuentes MMPB, Gillis AJ, Ceriani SA, Guttridge TL, Van Zinnicq Bergmann MPM, Smukall M, Gruber SH, Wildermann N (2019) Delineating Marine Protected areas in Bimini, Bahamas by considering hotspots for the green turtle (Chelonia mydas). Biodivers Conserv 28:197–211. https://doi.org/10.1007/s10531-018-1647-2

    Article  Google Scholar 

  27. Galbraith DA, Chandler MW, Brooks RJ (1987) The fine structure of home ranges of male Chelydra serpentina: are snapping turtles territorial? Can J Zool 65:2623–2629. https://doi.org/10.1139/z87-398

    Article  Google Scholar 

  28. Gillis AJ, Ceriani SA, Seminoff JA, Fuentes MMPB (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. https://doi.org/10.3354/meps12635

    CAS  Article  Google Scholar 

  29. Giroux MA, Dussault C, Lecomte N, Tremblay JP, Cote SD (2012) A new way of assessing forage behaviour at the individual level using faeces marking and satellite telemetry. PLoS ONE 7(11):e49719. https://doi.org/10.1371/jounral.pone.0049719

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  30. Gledhill KS, Kessel ST, Guttridge TL, Hansell AC, Bester-Van Der Merwe AE, Feldheim KA, Gruber SH, Chapman DD (2015) Genetic structure, population demography and seasonal occurrence of blacktip sharks Carcharhinus limbatus in Bimini, the Bahamas. J Fish Biol 87:1371–1388. https://doi.org/10.1111/jfb.12821

    CAS  Article  PubMed  Google Scholar 

  31. Gosch M, Cronin M, Rogan E, Hunt W, Luck C, Jessopp M (2019) Spatial Variation in a top marine predator’s diet at two regionally distinct sites. PLoS ONE 14(1):e0209032. https://doi.org/10.1371/journal.pone.0209032

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  32. Goshe LR, Avens L, Scharf FS, Southwood AL (2010) Estimation of age at maturation and growth of Atlantic green turtles (Chelonia mydas) using skeletochronology. Mar Biol 157:1725–1740. https://doi.org/10.1007/s00227-010-1446-0

    Article  Google Scholar 

  33. Gruber SH, Parks W (2002) Mega-resort development on Bimini: Sound economics or environmental disaster? Bahamas J Sci 9:2–18

    Google Scholar 

  34. Guttridge TL, Gruber SH, Franks BR, Kessel ST, Gledhill KS, Uphill J, Krause J, Sims DW (2012) Deep danger: Intra-specific predation risk influences habitat use and aggregation formation of juvenile lemon sharks Negaprion brevirostris. Mar Ecol Prog Ser 445:279–291. https://doi.org/10.3354/meps09423

    Article  Google Scholar 

  35. 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. https://doi.org/10.1007/s00442-006-0431-2

    Article  PubMed  Google Scholar 

  36. Hawkes LA, Witt MJ, Broderick AC, Coker JW, Coyne MS, Dodd M, Frick MG, Godfrey MH, Griffin DB, Murphy SR, Murphy TM, Williams KL, Godley BJ (2011) Home on the range: Spatial ecology of loggerhead turtles in Atlantic waters of the USA. Divers Distrib 17:624–640. https://doi.org/10.1111/j.1472-4642.2011.00768.x

    Article  Google Scholar 

  37. 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. https://doi.org/10.1007/s00227-012-2117-0

    Article  Google Scholar 

  38. Heady WN, Moore JW (2013) Tissue turnover and stable isotope clocks to quantify resource shifts in anadromous rainbow trout. Oecologia 172:21–34. https://doi.org/10.1007/s00442-012-2483-9

    Article  PubMed  Google Scholar 

  39. Hernández L, Laundré JW (2005) Foraging in the ‘landscape of fear’ and its implications for habitat use and diet quality of elk Cervus elaphus and bison Bison bison. Wildlife Biol 11:215–220. https://doi.org/10.2981/0909-6396(2005)11[215:FITLOF]2.0.CO;2

    Article  Google Scholar 

  40. Hobbs JPA, Munday PL (2004) Intraspecific competition controls spatial distribution and social organisation of the coral-dwelling goby Gobiodon histrio. Mar Ecol Prog Ser 278:253–259. https://doi.org/10.3354/meps278253

    Article  Google Scholar 

  41. Hoenner X, Whiting SD, Hindell MA, McMahon CR (2012) Enhancing the use of ARGOS satellite data for home range and long distance migration studies of marine animals. PLoS ONE. https://doi.org/10.1371/journal.pone.0040713

    Article  PubMed  PubMed Central  Google Scholar 

  42. Holloway-Adkins KG, Hanisak MD (2017) Macroalgal foraging preferences of juvenile green turtles (Chelonia mydas) in a warm water temperate/subtropical transition zone. Mar Biol 162:161–172. https://doi.org/10.1007/s00227-017-3191-0

    Article  Google Scholar 

  43. Hunt GL, Russell RW, Coyle KO, Weingartner T (1998) Comparative foraging ecology of planktivorous auklets in relation to ocean physics and prey availability. Mar Ecol Prog Ser 167:241–259. https://doi.org/10.3354/meps167241

    Article  Google Scholar 

  44. Hussey NE (2003) An evaluation of Landsat7 ETM+ satellite imagery for quantitative biotope mapping of the Bimini Islands, the Bahamas including two known lemon shark (Negaprion brevirostris) nursery grounds. MSc thesis, University of Wales, Bangor.

  45. Hussey NE, Kessel ST, Aarestrup K, Cooke SJ, Cowley PD, Fisk AT, Harcourrt RG, Holland KN, Iverson SJ, Kocik JF, Flemming JEM, Whoriskey FG (2015) Aquatic animal telemetry: a panoramic window into the underwater world. Ecol 348(6240):1255642. https://doi.org/10.1126/science.1255642

    CAS  Article  Google Scholar 

  46. Ivlev VS (1961) Experimental Ecology of the Feeding of Fishes. Yale University Press, New Haven

    Google Scholar 

  47. Jacobs J (1974) Quantitative measurement of food selection. Oecologia 14:413–417. https://doi.org/10.1007/BF00384581

    Article  PubMed  Google Scholar 

  48. Jennings DE, Gruber SH, Franks BR, Kessel ST, Robertson AL (2008) Effects of large-scale anthropogenic development on juvenile lemon shark (Negaprion brevirostris) populations of Bimini. Bahamas Environ Biol Fish 83(4):369–377. https://doi.org/10.1007/s10641-008-9357-3

    Article  Google Scholar 

  49. Jennings DE, DiBattista JD, Stump KL, Hussey NE, Franks BR, Grubbs RD, Gruber SH (2012) Assessment of the aquatic biodiversity of a threatened coastal lagoon at Bimini, Bahamas. J Coast Conserv 16:405–428. https://doi.org/10.1007/s11852-012-0211-6

    Article  Google Scholar 

  50. Johnson DH (1980) The comparison of usage and availability measurements for evaluating resource preference. Ecol 61:65–71. https://doi.org/10.2307/1937156

    Article  Google Scholar 

  51. Johnson RA, Gulick AG, Bolten AB, Bjorndal KA (2017) Blue carbon stores in tropical seagrass meadows maintained under green turtle grazing. Sci Rep 7:13545. https://doi.org/10.1038/s41598-017-13142-4

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  52. Jonsen ID, Myers RA, James MC (2006) Robust hierarchical state-space models reveal diel variation in travel rates of migrating leatherback turtles. J Anim Ecol 75:1046–1057. https://doi.org/10.1111/j.1365-2656.2006.01129.x

    Article  PubMed  Google Scholar 

  53. Jonsen ID, Basson M, Bestley S, Bravington MV, Patterson TA, Pedersen MW, Thomson R, Thygesen UH, Wotherspoon SJ (2013) State-space models for bio-loggers: a methodological road map. Deep Res Part II Top Stud Oceanogr 88–89:34–46. https://doi.org/10.1016/j.dsr2.2012.07.008

    Article  Google Scholar 

  54. Jonsen ID (2016) Joint estimation over multiple individuals improves behavioural state inference from animal movement data. Sci Rep 6:1–9. https://doi.org/10.1038/srep20625

    CAS  Article  Google Scholar 

  55. Kondoh M (2003) Foraging adaptation and the relationship between food web complexity and security. Science (80-) 299:1388–1391. https://doi.org/10.1126/science.1087539

    CAS  Article  Google Scholar 

  56. Lal A, Arthur R, Marba N, Lill AWT, Alcoverro T (2010) Implications of conserving an ecosystem modifier: Increasing green turtle (Chelonia mydas) densities substantially alters seagrass meadows. Biol Conserv 143:2730–2738. https://doi.org/10.1016/j.biocon.2010.07.020

    Article  Google Scholar 

  57. Lechowicz MJ (1982) The sampling characteristics of electivity indices. Oecologia 52:22–30. https://doi.org/10.1007/BF00349007

    Article  PubMed  Google Scholar 

  58. 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 Bio Ecol 405:25–32. https://doi.org/10.1016/j.jembe.2011.05.012

    Article  Google Scholar 

  59. Levin LA, Currin C (2012) Stable Isotope Protocols: Sampling and Sample Processing. UC San Diego: Scripps Institution of Oceanography. Retrieved from https://escholarship.org/uc/item/3jw2v1hh. Accessed 5 Dec 2016

  60. Li HW, Brocksen RW (1977) Approaches to the analysis of energetic costs of intraspecific competition for space by rainbow trout (Salmo gairdneri). J Fish Biol 11(4):329–341. https://doi.org/10.1111/j.1095-8649.1977.tb04126.x

    Article  Google Scholar 

  61. Lima AF, Tavares-Filho A, Moro GV (2018) Natural food intake by juvenile Arapaima gigas during the grow-out phase in earthen ponds. Aquac Res 49:2051–2058. https://doi.org/10.1111/are.13662

    Article  Google Scholar 

  62. Limpus CJ, Limpus DJ (2003) Biology of the loggerhead turtls in western south Pacific Ocean foraging areas. In: Witherington BE, Bolten AB (eds) Loggerhead sea turtles. Smithsonian Institution Press, Washington, DC, pp 93–113

    Google Scholar 

  63. López-Mendilaharsu M, Gardner SC, Riosmena-Rodriguez R, Seminoff JA (2008) Diet selection by immature green turtles (Chelonia mydas) at Bahía Magdalena foraging ground in the Pacific Coast of the Baja California Peninsula, México. J Mar Biol Assoc UK 88:1–7. https://doi.org/10.1017/S0025315408001057

    Article  Google Scholar 

  64. Makowski C, Seminoff JA, Salmon M (2006) Home range and habitat use of juvenile Atlantic green turtles (Chelonia mydas) on shallow reef habitats in Palm Beach, Florida, USA. Mar Biol 148:1167–1179. https://doi.org/10.1007/s00227-005-0150-y

    Article  Google Scholar 

  65. Månsson J, Andrén H, Pehrson Å, Bergström R (2007) Moose browsing and forage availability: a scale-dependent relationship? Can J Zool 85:372–380. https://doi.org/10.1139/Z07-015

    Article  Google Scholar 

  66. Mcconnell BJ, Chambers C, Fedak MA (1992) Foraging ecology of southern elephant seals in relation to the bathymetry and productivity of the Southern Ocean. Antarct Sci 4:393–398. https://doi.org/10.1017/S0954102092000580

    Article  Google Scholar 

  67. McIntyre T, Bester MN, Bornemann H, Tosh CA, de Bruyn PJN (2017) Slow to change? Individual fidelity to three-dimensional foraging habitats in southern elephant seals, Mirounga leonina. Anim Behav 127:91–99. https://doi.org/10.1016/j.anbehav.2017.03.006

    Article  Google Scholar 

  68. McMahon LA, Rachlow JL, Shipley LA, Forbey JS, Johnson TR (2017) Habitat selection differs across hierarchical behaviors: Selection of patches and intensity of patch use. Ecosphere 8(11):e01993. https://doi.org/10.1002/ecs2.1993

    Article  Google Scholar 

  69. Moran KL, Bjorndal KA (2007) Simulated green turtle grazing affects nutrient composition of the seagrass Thalassia testudinum. Mar Biol 150:1083–1092. https://doi.org/10.1007/s00227-006-0427-9

    CAS  Article  Google Scholar 

  70. Mumby PJ, Green EP, Clark CD, Edwards AJ (1998) Digital analysis of multispectral airborne imagery of coral reefs. Coral Reefs 17:59–69. https://doi.org/10.1007/s003380050096

    Article  Google Scholar 

  71. Mumby PJ, Edwards AJ (2002) Mapping marine environments with IKONOS imagery: Enhanced spatial resolution can deliver greater thematic accuracy. Remote Sens Environ 82:248–257. https://doi.org/10.1016/S0034-4257(02)00041-X

    Article  Google Scholar 

  72. Norbury GL, Sanson GD (1992) Problems with measuring diet selection of terrestrial, mammalian herbivores. Aust J Ecol 17(1):1–7. https://doi.org/10.1111/j.1442-9993.1992.tb00774.x

    Article  Google Scholar 

  73. Owen-Smith N, Fryxell JM, Merrill EH (2010) Foraging theory upscaled: the behavioural ecology of herbivore movement. Philos Trans R Soc B Biol Sci 365:2267–2278. https://doi.org/10.1098/rstb.2010.0095

    CAS  Article  Google Scholar 

  74. Pankratz C (1995) PREFER: statistical package for comparisons of resource preference. US Fish and Wildlife Services, Northern Prairie Research Center, Jamestown, ND

  75. Parnell AC, Phillips DL, Bearhop S, Semmens BX, Ward EJ, Moore JW, Jackson AL, Grey J, Kelly DJ, Inger R (2013) Bayesian stable isotope mixing models. Environmetrics 24:387–399. https://doi.org/10.1002/env.2221

    Article  Google Scholar 

  76. Phillips DL (2001) Mixing models in analyses of diet using multiple stable isotopes: a critique. Oecologia 127:166–170. https://doi.org/10.1007/s004420000571

    Article  PubMed  Google Scholar 

  77. Phillips DL, Gregg JW (2001) Uncertainty in source partitioning using stable isotopes. Oecologia 127:171–179. https://doi.org/10.1007/s004420000578

    Article  PubMed  Google Scholar 

  78. Pyke GH (1984) Optimal foraging theory: a critical review. Annu Rev Ecol Syst 15:523–575

    Article  Google Scholar 

  79. Rahman MM, Kadowaki S, Balcombe SR, Wahab MA (2010) Common carp (Cyprinus carpio L.) alters its feeding niche in response to changing food resources: Direct observations in simulated ponds. Ecol Res 25:303–309. https://doi.org/10.1007/s11284-009-0657-7

    Article  Google Scholar 

  80. Reich KJ, Bjorndal KA, Bolten AB (2007) The “lost years” of green turtles: using stable isotopes to study cryptic lifestages. Biol Lett 3:712–714. https://doi.org/10.1098/rsbl.2007.0394

    Article  PubMed  PubMed Central  Google Scholar 

  81. Renaud ML, Carpenter JA, Williams JA, Manzella-Tirpak SA (1995) Activities of juvenile green turtles, Chelonia mydas, at a jettied pass in south Texas. Fish Bull 93:586–593

    Google Scholar 

  82. Rotjan RD, Lewis SM (2006) Parrotfish abundance and selective corallivory on a Belizean coral reef. J Exp Mar Bio Ecol 335:292–301. https://doi.org/10.1016/j.jembe.2006.03.015

    Article  Google Scholar 

  83. Sampson L, Giraldo A, Payán LF, Amorocho DF, Ramos MA, Seminoff JA (2017) Trophic ecology of green turtle Chelonia mydas juveniles in the Colombian Pacific. J Mar Biol Assoc UK 98(7):1817–1829. https://doi.org/10.1017/S0025315417001400

    Article  Google Scholar 

  84. Schofield G, Bishop CM, MacLean G, Brown P, Baker M, Katselidis KA, Dimopoulos P, Pantis JD, Hays GC (2007) Novel GPS tracking of sea turtles as a tool for conservation management. J Exp Mar Bio Ecol 347:58–68. https://doi.org/10.1019/j.jembe.2007.03.009

    Article  Google Scholar 

  85. Seminoff JA, Resendiz A, Nichols WJ (2002) Home range of green turtles Chelonia mydas at a coastal foraging area in the Gulf of California, Mexico. Mar Ecol Prog Ser 242:253–265. https://doi.org/10.3354/meps242253

    Article  Google Scholar 

  86. 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. https://doi.org/10.3354/meps308271

    CAS  Article  Google Scholar 

  87. Senft R, Coughenour M, Bailiey D, Rittenhouse L, Sala O, Swift D (1987) Large herbivore foraging and ecological hierarchies. Bioscience 37:789–795. https://doi.org/10.2307/1310545

    Article  Google Scholar 

  88. Sheppard CRC, Matheson K, Bythell JC, Murphy P, Myers CB, Blake B (1995) Habitat mapping in the Caribbean for management and conservation: Use and assessment of aerial photography. Aquat Conserv Mar Freshw Ecosyst. https://doi.org/10.1002/aqc.3270050404

    Article  Google Scholar 

  89. Shillinger GL, Swithenbank AM, Bailey H, Bograd SJ, Castelton MR, Wallace BP, Spotila JR, Paladino FV, Piedra R, Block BA (2011) Vertical and horizontal habitat preferences of post-nesting leatherback turtles in the South Pacific Ocean. Mar Ecol Prog Ser 422:275–289. https://doi.org/10.3354/meps08884

    Article  Google Scholar 

  90. Shimada T, Limpus C, Jones R, Hazel J, Groom R, Hamann M (2016) Sea turtles return home after intentional displacement from coastal foraging areas. Mar Biol 163:1–14. https://doi.org/10.1007/s00227-015-2771-0

    CAS  Article  Google Scholar 

  91. Shipley LA, Blomquist S, Danell K (1998) Diet choices made by free-ranging moose in northern Sweden in relation to plant distribution, chemistry, and morphology. Can J Zool 76:1722–1733. https://doi.org/10.1139/z98-110

    Article  Google Scholar 

  92. Simcharoen A, Savini T, Gale GA, Simcharoen S, Duangchantrasiri S, Pakpien S, Smith JLD (2014) Female tiger Panthera tigris home range size and prey abundance: Important metrics for management. Oryx 48:370–377. https://doi.org/10.1017/S0030605312001408

    Article  Google Scholar 

  93. Simmons R, Barnard P, MacWhirter B, Hansen GL (1986) The influence of microtines on polygyny, productivity, age, and provisioning of breeding Northern Harriers: a 5-year study. Can J Zool 64:2447–2456. https://doi.org/10.1139/z86-365

    Article  Google Scholar 

  94. Simpson SJ, Sibly RM, Lee KP, Behmer ST, Raubenheimer D (2004) Optimal foraging when regulating intake of multiple nutrients. Anim Behav 68:1299–1311. https://doi.org/10.1016/j.anbehav.2004.03.003

    Article  Google Scholar 

  95. Stock B, Semmens B (2016) MixSIAR (GUI user manual). Version 3:1

    Google Scholar 

  96. Strauss RE (1979) Reliability estimates for Ivlev’s electivity index, the forage ratio, and a proposed linear index of food selection. Trans Am Fish Soc 108:344–352. https://doi.org/10.1577/1548-8659(1979)108%3c344:REFIRI%3e2.0.CO;2

    Article  Google Scholar 

  97. Stump KL (2013) The effects of nusery habitat loss on juvenile lemon sharks, Negaprion brevirostris. Ph.D dissertation, University of Miami, Coral Gables, FL

  98. Sugden LG (1969) Foods, food selection, and energy requirements of wild ducklings in Southern Alberta. Ph.D dissertation, Utah State University, Logan

  99. Thayer GW, Bjorndal KA, Ogden JC, Williams SL, Zieman JC (1984) Role of larger herbivores in seagrass communities. Estuaries 7:351–376. https://doi.org/10.2307/1351619

    Article  Google Scholar 

  100. Thompson AR, Todd Petty J, Grossman GD (2001) Multi-scale effects of resource patchiness on foraging behaviour and habitat use by longnose dace, Rhinichthys cataractae. Freshw Biol 46:145–160. https://doi.org/10.1046/j.1365-2427.2001.00654.x

    Article  Google Scholar 

  101. Thomson JA, Gulick A, Heithaus MR (2015) Intraspecific behavioral dynamics in a green turtle Chelonia mydas foraging aggregation. Mar Ecol Prog Ser 532:243–256. https://doi.org/10.3354/meps11346

    Article  Google Scholar 

  102. Tieszen LL, Boutton TW, Tesdahl KG, Slade NA (1983) Fractionation and turnover of stable carbon isotopes in animal tissues: Implications for δ13C analysis of diet. Oecologia 57:32–37. https://doi.org/10.1007/BF00379558

    CAS  Article  PubMed  Google Scholar 

  103. van Beest FM, Mysterud A, Loe LE, Milner JM (2010) Forage quantity, quality and depletion as scaledependent mechanisms driving habitat selection of a large browsing herbivore. J Anim Ecol 79:910–922. https://doi.org/10.1111/j.1365-2656.2010.01701.x

    Article  PubMed  Google Scholar 

  104. Vander Zanden HB, Bjorndal KA, Reich KJ, Bolten AB (2010) Individual specialist in a generalist population: results from long-term stable isotope series. Biol Letters 6:711–714. https://doi.org/10.1098/rsbl.2010.0124

    Article  Google Scholar 

  105. Vander Zanden HB, Arthur KE, Bolten AB, Popp BN, Lagueux CJ, Harrison E, Campbell CL, Bjorndal KA (2013) Trophic ecology of a green turtle breeding population. Mar Ecol Prog Ser 476:237–249. https://doi.org/10.3354/meps10185

    Article  Google Scholar 

  106. Viejou R, Avgar T, Brown GS, Patterson BR, Reid DEB, Rodgers AR, Shuter J, Thompson ID (2018) Fryxell JM (2018) Woodland caribou habitat selection patterns in relation to predation risk and forage abundance depend on reproductive state. Ecol Evol 8:5863–5872. https://doi.org/10.1002/ece3.4124

    Article  PubMed  PubMed Central  Google Scholar 

  107. Waller RA, Duncan DB (1969) A Bayes rule for the symmetric multiple comparisons problem. J Am Stat Assoc 64:1484–1503. https://doi.org/10.1080/01621459.1969.10501073

    Article  Google Scholar 

  108. Wildermann NE, Gredzens C, Avens L, Héctor A, Bell I, Blumenthal J, Bolten AB, Mcneill JB, Casale P, Di DM, Domit C, Epperly SP, Matthew H, Godley BJ, Carman VG, Hamann M, Kristen M, Ishihara T, Mansfield KL, Metz TL, Miller JD, Nicolas J, Read MA, Sasso C, Seminoff JA, Seney EE, Williard AS, Tomás J, Vélez-rubio GM, Williams JL, Wyneken J, Fuentes MMPB (2018) Informing research priorities for immature sea turtles through expert elicitation. Endanger Species Res 37:55–76. https://doi.org/10.3354/esr00916

    Article  Google Scholar 

  109. Zeh DR, Heupel MR, Limpus CJ, Hamman M, Fuentes MMPB, Babcock RC, Pillans RD, Townsend KA, Marsh H (2015) Is acoustic tracking appropriate for air-breathing marine animals? Dugongs as a case study. J Exp Mar Biol Ecol 464:1–10. https://doi.org/10.1016/j.jembe.2014.11.013

    Article  Google Scholar 

  110. Zweifel-Schielly B, Leuenberger Y, Kreuzer M, Suter W (2012) A herbivore’s food landscape: seasonal dynamics and nutritional implications of diet selection by red deer population in contrasting Alpine habitats. J Zool 286:68–80. https://doi.org/10.1111/j.1469-7998.2011.00853.x

    Article  Google Scholar 

Download references

Acknowledgements

We are grateful to National Geographic, Save our Seas Foundation and the Florida State University Council on Research and Creativity for their contributions towards funding this study. We are also grateful to Dr. Samuel Gruber, Dr. Tristan Guttridge, the managers and volunteers from Bimini Biological Field Station Foundation for their assistance with logistics during field work. Further, we are grateful to Dr. Camila Domit at Universidade Federal do Prana and Christian Gredzens for their assistance in field sampling. Our gratitude is also extended to Ethan Goddard from the Paleoclimatology, Paleoceanography and Biogeochemistry Laboratory at the University of South Florida College of Marine Science, Susan Murasko from Florida Fish and Wildlife Research Institute, Florida Fish and Wildlife Conservation Commission, Garrett Lemons and Joel Schumacher from the NOAA-Southwest Fisheries Service Center for their assistance in sample preparation and analysis. We are grateful to Erin LaCasella and Gabriela Serra-Valente from NOAA-Southwest Fisheries Service Center for their assistance with CITES importation. We would also like to thank Ian Silver-Gorges, journal reviewers and editor for assisting in the editorial process and helping ready this manuscript for publication.

Funding

Funding for this project was provided by National Geographic (CS 203_16), Save Our Sea Foundation and the Florida State University Council on Research and Creativity.

Author information

Affiliations

Authors

Contributions

Mr. AJG conducted the field sampling, stable isotope preparations, data analysis and has served as the primary author in the preparation of this manuscript. Dr. NEW guided Mr. AJG in preparing, cleaning and analyzing the satellite telemetry data utilized in this study. She provided a general schema and code base to be used for location cleaning. Dr. NEW also contributed to several rounds of manuscript edits throughout the preparation of this manuscript. Dr. SAC contributed to the field sampling efforts conducted in this manuscript. She also provided invaluable guidance and logistics for carrying stable isotope sample preparations and analysis. Dr. SAC also provided edits for the preparation of this manuscript. Dr. JAS provided insights on the use the selected stable isotope mixing model as well as the application of diet selection indices in this study. He also assisted in field sampling, stable isotope analysis and provided several rounds of edits for the preparation of this manuscript. Dr. MPBF assisted in field sampling and served as Mr. AJG academic advisor as this research was carried out during his tenure as a graduate research assistant. She also provided edits throughout the preparation of this manuscript.

Corresponding author

Correspondence to Mariana M. P. B. Fuentes.

Ethics declarations

Conflicts of interest/Competing interest

Further, there are no conflicts of or competing interests associated with this project or manuscript preparation.

Ethical approval

Sampling carried out for this project was permitted under the Bahamian research permits (MAMR/LIA/22) and Florida State University Institutional Animal Care and Use Committee permit (Protocol #1521). All sampling techniques and out-of-water handling times, as set out in the IACUC permit, were strictly followed ensuring the proper care of each individual turtle sampled. Further, international transportation of endangered species samples was permitted under the Convention on International Trade in Endangered Species permit (USFWS CITES Import Permit #16US844694/9 and Bahamas CITES Export Permit #2016/516).

Informed consent

Consent for participation is not applicable to this study as there were no human test subjects.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

L. Sampson and an undisclosed expert.

Responsible Editor: L. Avens.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 179 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Gillis, A.J., Wildermann, N.E., Ceriani, S.A. et al. Evaluating different spatial scales of forage item availability to determine diet selection of juvenile green turtles (Chelonia mydas). Mar Biol 167, 170 (2020). https://doi.org/10.1007/s00227-020-03782-y

Download citation