Abstract
Young green turtles (Chelonia mydas) spend their early lives as oceanic omnivores with a prevalence of animal prey. Once they settle into neritic habitats (recruitment), they are thought to shift rapidly to an herbivorous diet, as revealed by studies in the Greater Caribbean. However, the precise timing of the ontogenic dietary shift and the actual relevance of animal prey in the diet of neritic green turtles are poorly known elsewhere. Stable isotopes of carbon, sulfur and nitrogen in the carapace scutes of 19 green turtles from Mauritania (NW Africa), ranging from 26 to 102 cm in curved carapace length (CCLmin), were analyzed to test the hypothesis of a rapid dietary shift after recruitment. Although the length of residence time in neritic habitats increased with turtle length, as revealed by a significant correlation between turtle length and the δ13C and the δ34S of the scutes, comparison of the δ15N of the innermost and outermost layers of carapace scutes demonstrated that consumption of macrophytes did not always start immediately after recruitment, and turtles often resumed an animal-based diet after starting to graze on seagrasses. As a consequence, seagrass consumption did not increase gradually with turtle size and animal prey largely contributed to the diet of turtles within the range 29–59 cm CCLmin (76–99% of assimilated nutrients). Seagrass consumption by turtles larger than 59 cm CCLmin was higher, but they still relied largely on animal prey (53–76% of assimilated nutrients). Thus, throughout most of their neritic juvenile life, green turtles from NW Africa would be better classified as omnivores rather than herbivores.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Amorocho D, 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. doi:https://doi.org/10.3354/esr003043
Ayliffe LK, Cerling TE, Robinson T, West AG, Sponheimer M, Passey BH, Hammer J, Roeder B, Dearing MD, Ehleringer JR (2004) Turnover of carbon isotopes in tail hair and breath CO2 of horses fed an isotopically varied diet. Oecologia 139:11–22. doi:https://doi.org/10.1007/s00442-003-1479-x
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 (Berl) 145:1043–1059. doi:https://doi.org/10.1007/s00227-004-1387-6
Balguerias Guerra E (1997) Discards in fisheries from the eastern central Atlantic (CECAF region). FAO Fish report 547 suppl
Bjorndal KA (1979) Cellulose digestion and volatile fatty acid production in the green turtles, Chelonia mydas. Comp Biochem Physiol 63A:127–133. doi:https://doi.org/10.1016/0300-9629(79)90638-8
Bjorndal KA (1980) Nutrition and grazing behaviour of the green turtle Chelonia mydas. Mar Biol (Berl) 56:147–154. doi:https://doi.org/10.1007/BF00397131
Bjorndal KA (1985) Nutritional ecology of sea turtles. Copeia 1985:736–751. doi:https://doi.org/10.2307/1444767
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 199–232
Bjorndal KA, Bolten AB (1988) Growth rates of immature green turtles, Chelonia mydas, on feeding grounds in the southern Bahamas. Copeia 1988:555–564. doi:https://doi.org/10.2307/1445373
Bjorndal KA, Jackson JBC (2003) Roles of sea turtles in marine ecosystems: reconstructing the past. In: Lutz PL, Musick JA (eds) The biology of sea turtles. CRC Press, Boca Raton, pp 259–273
Bjorndal KA, Bolten AB, Chaloupka MY (2000) Green turtle somatic growth model: evidence for density dependence. Ecol Appl 10:269–289
Cardona L, Revelles M, Sales M, Aguilar A, Borrell A (2007) The meadows of the seagrass Posidonia oceanica are a relevant source of organic matter for adjoining ecosystems. Mar Ecol Prog Ser 335:123–131. doi:https://doi.org/10.3354/meps335123
Cebrian J (1999) Patterns in the fate of production in plant communities. Am Nat 154:449–468. doi:https://doi.org/10.1086/303244
Chaloupka M, Limpus C, Miller J (2004) Green turtle somatic growth dynamics in a spatially disjunct Great Barrier reef metapopulation. Coral Reefs 23:325–335. doi:https://doi.org/10.1007/s00338-004-0387-9
DeNiro MJ, Epstein S (1978) Influence of diet on the distribution of carbon isotopes in animals. Geochim Cosmochim Acta 42:495–506. doi:https://doi.org/10.1016/0016-7037(78)90199-0
DeNiro MJ, Epstein S (1981) Influence of diet on the distribution of nitrogen isotopes in animals. Geochim Cosmochim Acta 45:341–351. doi:https://doi.org/10.1016/0016-7037(81)90244-1
Evans-White M, Dodds WK, Gray LJ, Fritz KM (2001) A comparison of the trophic ecology of the crayfishes (Orconectes nais [Faxon] and Orconectes neglectus [Faxon]) and the central stoneroller minnow (Campostoma anomalum (Rafinesque)): omnivory in a tallgrass prairie stream. Hydrobiologia 462:131–144. doi:https://doi.org/10.1023/A:1013182100150
Fantle MS, Dittel AI, Schwalm S, Epifanio CE, Fogel ML (1999) A food web analysis of the juvenile crab Callinectes sapidus, using stable isotopes in whole animals and individual amino acids. Oecologia 120:416–426. doi:https://doi.org/10.1007/s004420050874
Ferreira B, Garcia M, Jupp BP, Al-Kryumi A (2006) Diet of the green turtle (Chelonia mydas) at Ra’s Hadd, Sultanate of Oman. Chelon Conserv Biol 5(1):141–145
Forcada J, Hammond PS, Aguilar A (1999) Status of the Mediterranean monk seal Monachus monachus in the Western Sahara and the implications of a mass mortality event. Mar Ecol Prog Ser 188:249–261. doi:https://doi.org/10.3354/meps188249
France RL, Peters RH (1997) Ecosystem differences in the trophic enrichment of 13C in aquatic food webs. Can J Fish Aquat Sci 54:1255–1258. doi:https://doi.org/10.1139/cjfas-54-6-1255
Fretey J (2001) Biogéographie et conservation des tortues marines de le côte atlantique de l’Afrique. CMS Technical Series Publication 6. UNEP/CMS Secretariat, Bonn
Gaye-Siessegger J, Focken U, Muetzel S, Abel H, Becker K (2004) Feeding level and individual metabolic rate affect δ13C and δ15N values in carp: implications for food web studies. Oecologia 138:175–183. doi:https://doi.org/10.1007/s00442-003-1429-7
Godley BJ, Thompson DR, Waldron S, Furness RW (1998) The trophic status of marine turtles as determined by stable isotope analysis. Mar Ecol Prog Ser 166:277–284. doi:https://doi.org/10.3354/meps166277
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. doi:https://doi.org/10.1007/s00442-006-0431-2
Heithaus MR, McLash JJ, Frid A, Dill LM, Mashall GJ (2002) Novel insights into green sea turtle behaviour using animal-borne video cameras. J Mar Biol Assoc UK 82:1049–1050. doi:https://doi.org/10.1017/S0025315402006689
Hemminga MA, Duarte C (2000) Seagrass ecology. Cambridge University Press, Cambridge
Hemminga MA, Nieuwenhuize J (1991) Transport, deposition and in situ decay of seagrasses in a tropical mudflat area (Band d’Arguin, Mauritania). Neth J Sea Res 27:183–190. doi:https://doi.org/10.1016/0077-7579(91)90011-O
Hobson KA, Clark RG (1992) Assessing avian diets using stable isotopes II: factors influencing diet-tissue fractionation. Condor 94:189–197. doi:https://doi.org/10.2307/1368808
Hobson KA, Schell DM, Renouf D, Noseworthy E (1996) Stable carbon and nitrogen isotopic fractionation between diet and tissues of captive seals: implications for dietary reconstruction involving marine mammals. Can J Fish Aquat Sci 53:528–533. doi:https://doi.org/10.1139/cjfas-53-3-528
Kobayashi M (2001) Annual cycle of the speckle pattern on the carapace of immature hawksbill turtles (Eretmochelys imbricata) in Cuba. Amphib-reptil 22:321–328. doi:https://doi.org/10.1163/156853801317050115
Laan BBPA, van der Wolff WJ (2006) Circular pools in the seagrass beds of the Banc d’Arguin, Mauritania, and their possible origin. Aquat Bot 84:93–100. doi:https://doi.org/10.1016/j.aquabot.2005.07.009
Lanyon JM, Limpus CJ, Marsh H (1989) Dugongs and turtles: grazers in the seagrass system. In: Larkum AWK, McComb AJ, Shepherd SA (eds) Biology of seagrasses. Elsevier, Amsterdam, pp 610–634
Lepoint G, Nyssen F, Gobert S, Dauby P, Bouquegneau J-M (2000) Relative impact of a seagrass bed and its adjacent epilithic algal community in consumer diets. Mar Biol (Berl) 136:513–518. doi:https://doi.org/10.1007/s002270050711
Limpus CJ, Couper PJ, Read MA (1994) The green turtle, Chelonia mydas, in Queensland: population structure in a warm temperate feeding area. Mem Queensl Mus 35:139–154
McCutchan JH, Lewis WM, Kendall K, McGrath CC (2003) Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos 102:378–390. doi:https://doi.org/10.1034/j.1600-0706.2003.12098.x
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. doi:https://doi.org/10.1016/0016-7037(84)90204-7
Moran KL, Bjorndal KA (2005) Simulated green turtle grazing affects structure and productivity of seagrass pastures. Mar Ecol Prog Ser 305:235–247. doi:https://doi.org/10.3354/meps305235
Mortimer JA (1981) The feeding ecology of the Western Caribbean green turtle, Chelonia mydas, in Nicaragua. Biotropica 13:49–58. doi:https://doi.org/10.2307/2387870
Nieri M, Grau E, Lamarche B, Aguilar A (1999) Mass mortality of Atlantic spotted dolphins (Stenella frontalis) caused by a fishing interaction in Mauritania. Mar Mamm Sci 15:847–854. doi:https://doi.org/10.1111/j.1748-7692.1999.tb00847.x
Phillips DL, Gregg JW (2003) Source partitioning using stable isotopes: coping with too many sources. Oecologia 136:261–269. doi:https://doi.org/10.1007/s00442-003-1218-3
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. doi:https://doi.org/10.1098/rsbl.2007.0394
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. doi:https://doi.org/10.1007/s00442-007-0949-y
Revelles M, Cardona L, Aguilar A, Fernández G (2007a) The diet of oceanic loggerhead sea turtles Caretta caretta off the Balearic archipelago (western Mediterranean): relevance of long-line baits. J Mar Biol Assoc UK 87:805–813. doi:https://doi.org/10.1017/S0025315407054707
Revelles M, Cardona L, Aguilar A, Borrell A, Fernández G, San Félix M (2007b) Concentration of stable C and N isotopes in several tissues of the loggerhead sea turtle Caretta caretta from the western Mediterranean and dietary implications. Sci Mar 71:87–93. doi:https://doi.org/10.3989/scimar.2007.71n187
Roth JD, Hobson KA (2000) Stable carbon and nitrogen isotopic fractionation between diet and tissue of captive red fox: implications for dietary reconstruction. Can J Zool 78:848–852. doi:https://doi.org/10.1139/cjz-78-5-848
Seminoff JA, Resendiz A, Nichols WJ (2002) Diet of the east Pacific green turtle, Chelonia mydas, in the central Gulf of California, Mexico. J Herpetol 36:447–453
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. doi:https://doi.org/10.3354/meps308271
Sullivan MJ, Moncreiff CA (1990) Edaphic algae are important components of salt mash food webs: evidence from multiple stable isotope analyses. Mar Ecol Prog Ser 62:149–159. doi:https://doi.org/10.3354/meps062149
Valentine JF, Duffy JE (2006) The central role of grazing in seagrass ecology. In: Larkum WD, Orth RJ, Duarte C (eds) Seagrasses: biology, ecology and conservation. Springer, Dordrecht, pp 463–501
Valentine JF, Heck JL (1999) Seagrass herbivory, evidence for the continued grazing of marine grasses. Mar Ecol Prog Ser 176:291–302. doi:https://doi.org/10.3354/meps176291
Van der Klift MA, Ponsard S (2003) Sources of variation in consumer-diet delta N-15 enrichment: a meta-analysis. Oecologia 136:169–182. doi:https://doi.org/10.1007/s00442-003-1270-z
Vermaat JE, Beijer JAJ, Gijlstra R, Hootsmans MJM, Philippart CJM, van den Brink NW, van Vierseen W (1993) Leaf dynamics and standing stocks of intertidal Zostera noltii Hornem and Cymodocea nodosa (Ucria) Ascherson on the Banc d’Arguin (Mauritania). Hydrobiologia 258:59–72. doi:https://doi.org/10.1007/BF00006186
Vizzini S, Mazzola A (2003) Seasonal variations in the stable carbon and nitrogen isotope ratios (13C/12C and 15N/14N) of primary producers and consumers in a western Mediterranean coastal lagoon. Mar Biol (Berl) 142:1009–1018
Wallace BP, Seminoff JA, Kilham SS, Spotila JR, Dutton PH (2006) Leatherback turtles as oceanic indicators: stable isotope analyses reveal a trophic dichotomy between ocean basins. Mar Biol (Berl) 149:953–960. doi:https://doi.org/10.1007/s00227-006-0247-y
Wolff WJ, van der Land J, Nienhius PH, de Wilde PAWJ (1993) Ecological studies in the coastal waters of Mauritania. Preface. Hydrobiologia 358:vii–ix. doi:https://doi.org/10.1007/BF00006180
Zeeberg J, Corten A, De Graff E (2006) Bycath and release of pelagic megafauna in industrial trawler fisheries off Northwestern Africa. Fish Res 78:186–195. doi:https://doi.org/10.1016/j.fishres.2006.01.012
Zug GR, Glor RF (1999) Estimates of age and growth in a population of green seaturtles Chelonia mydas from the Indian River lagoon system, Florida: a skeletochronological analysis. Can J Zool 76:1497–1506. doi:https://doi.org/10.1139/cjz-76-8-1497
Zug GR, Balazs GH, Wetherall JA, Parker DM, Murakawa SKK (2001) Age and growth of Hawaiian green seaturtles (Chelonia mydas): an analysis based on skeletochronology. Fish Bull (Wash DC) 100:117–127
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by J.P. Grassle.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Cardona, L., Aguilar, A. & Pazos, L. 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 (2009). https://doi.org/10.1007/s00227-009-1188-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00227-009-1188-z