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Marine Biology

, 166:101 | Cite as

Dietary ontogeny of the blue shark, Prionace glauca, based on the analysis of δ13C and δ15N in vertebrae

  • Colombo Estupiñán-Montaño
  • Felipe Galván-MagañaEmail author
  • Alberto Sánchez-González
  • Fernando R. Elorriaga-Verplancken
  • Antonio Delgado-Huertas
  • Diego Páez-Rosas
Original Paper

Abstract

Ontogenetic changes in habitat and food preferences are common in nature; they reflect changes in the needs of organisms during their lifetime. Studying the dietary ontogeny of pelagic species is a difficult task, because of migratory processes and the inaccessibility of their habitats. As a result, their life history remains poorly understood, or even unknown. Here, we studied the dietary ontogeny of 18 blue sharks, Prionace glauca, using isotopic analysis in vertebrae. A total of 132 samples of vertebral collagen were taken (64 from males and 68 from females). The wide range of δ13C values (− 16.8 to − 13.1‰) suggests that these sharks use both coastal and oceanic areas for feeding. Small juveniles and adults preferred coastal areas, while medium-sized and large juveniles preferred oceanic areas. The estimated δ15N values (9.5–19.0‰) suggest that P. glauca is a top predator that occupies various trophic levels and/or it feeds across areas with different baseline δ15N (trophic position 3.9–8.4). Isotopic enrichment and differences in δ13C and δ15N thus suggest ontogenetic changes in habitat use and prey consumption between maturity stages. The use of hard anatomical structures (vertebrae) is highly relevant because they integrate information on the dietary ontogeny of this shark species.

Notes

Acknowledgements

CEM thanks the Galápagos Marine Reserve, Universidad San Francisco de Quito (Galápagos Campus), Instituto Andaluz de Ciencias de la Tierra, Instituto Politécnico Nacional’s Centro Interdisciplinario de Ciencias Marinas (CICIMAR-IPN), Consejo Nacional de Ciencia y Tecnología (CONACyT) and Fundación Alium Pacific. FGM, ASG, and FEV thank Instituto Politécnico Nacional for fellowships (Estímulo al Desempeño de los Investigadores [EDI] and Comisión para el Fomento de Actividades Académicas [COFAA]). We thank Isabelle Gamache and Erick García-García for editing the English text.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All sampling and experimental procedures performed in this study comply with the current Ecuadorian legislation.

References

  1. Baum JK, Worm B (2009) Cascading top-down effects of changing oceanic predator abundances. J Anim Ecol 78:699–714.  https://doi.org/10.1111/j.1365-2656.2009.01531.x CrossRefPubMedGoogle Scholar
  2. Baum JK, Myers RA, Kehler DG, Worm B, Harley SJ, Doherty PA (2003) Collapse and conservation of shark populations in the northwest Atlantic. Science 299(5605):389–392.  https://doi.org/10.1126/science.1079777 CrossRefPubMedGoogle Scholar
  3. Blanco-Parra MP, Galván-Magaña F, Márquez-Farías F (2008) Age and growth of the blue shark, Prionace glauca Linnaeus, 1758, in the Northwest coast off Mexico. Rev Biol Mar Oceanogr 43(3):513–520.  https://doi.org/10.4067/S0718-19572008000300010 CrossRefGoogle Scholar
  4. Briones-Mendoza J, Pincay-Espinosa J, Palma-Chávez J, Romero-Caicedo A (2016) Notas sobre la biología del tiburón azul Prionace glauca (Carcharhiniformes: Carcharhinidae) en aguas ecuatorianas. Rev Mex Biodivers 87(2016):1387–1390.  https://doi.org/10.1016/j.rmb.2016.09.007 CrossRefGoogle Scholar
  5. Carey FG, Scharold JV, Kalmijn AJ (1990) Movements of blue sharks (Prionace glauca) in depth and course. Mar Biol 106(3):329–342.  https://doi.org/10.1007/BF01344309 CrossRefGoogle Scholar
  6. Carlisle AB, Goldman KJ, Litvin SY, Madigan DJ, Bigman JS, Swithenbank AM, Kline TC Jr, Block BA (2015) Stable isotope analysis of vertebrae reveals ontogenetic change in hábitat in an endothermic pelagic shark. Proc R Soc B 282:20141446.  https://doi.org/10.1098/rspb.2014.1446 CrossRefPubMedGoogle Scholar
  7. Carrera-Fernández M, Galván-Magaña F, Ceballos-Vázquez BP (2010) Reproductive biology of the blue shark Prionace glauca (Chondrichthyes: Carcharhinidae) off Baja California Sur. México. Aqua 16(3):101–110Google Scholar
  8. Cortés E (1999) Standardized diet composition and trophic levels of sharks. ICES J Mar Sci 56(5):707–717.  https://doi.org/10.1006/jmsc.1999.0489 CrossRefGoogle Scholar
  9. Cortés E (2002) Incorporating uncertainty into demographic modeling: application to shark populations and their conservation. Conserv Biol 16(4):1048–1062.  https://doi.org/10.1046/j.1523-1739.2002.00423.x CrossRefGoogle Scholar
  10. Cruz-Ramírez A, Soriano-Velásquez SR, Santana-Hernández H, Ramírez-Santiago CE, Acal-Sánchez DE (2012) Aspectos reproductivos del tiburón azul Prionace glauca capturado por la flota palangrera de mediana altura del Puerto de Manzanillo, Colima. Ciencia Pesquera 20(1):39–48Google Scholar
  11. Duarte CM, Delgado-Huertas A, Anton A, Carrillo-de-Albornoz P, López-Sandoval DC, Agustí S, Almahasheer H, Marbá N, Hendriks IE, Krause-Jensen D, Garcias-Bonet N (2018) Stable isotope (δ13C, δ15N, δ18O, δD) composition and nutrient concentration of Red Sea primary producers. Front Mar Sci 5:1–12.  https://doi.org/10.3389/fmars.2018.00298 CrossRefGoogle Scholar
  12. Dulvy NK, Baum JK, Clarke S, Compagno LJV, Cortés E, Domingo A, Fordham S, Fowler S, Francis MP, Gibson C, Martínez J, Musick JA, Soldo A, Stevens JD, Valenti S (2008) You can swim but you can’t hide: the global status and conservation of oceanic pelagic sharks and rays. Aquat Conserv Mar Freshw Ecosyst 18(5):459–482.  https://doi.org/10.1002/aqc.975 CrossRefGoogle Scholar
  13. Elorriaga-Verplancken F, Aurioles-Gamboa D, Newsome SD, Martínez-Díaz SF (2013) δ15N and δ13C values in dental collagen as a proxy for age- and sex-related variation in foraging strategies of California sea lions. Mar Biol 160:641–652.  https://doi.org/10.1007/s00227-012-2119-y CrossRefGoogle Scholar
  14. Estrada JA, Rice AN, Lutcavage ME, Skomal GB (2003) Predicting trophic position in sharks of the north–west Atlantic Ocean using stable isotopes analysis. J Mar Biol Assoc UK 83(6):1347–1350.  https://doi.org/10.1017/S0025315403008798 CrossRefGoogle Scholar
  15. Estrada JA, Rice AN, Natason LJ, Skomal GB (2006) Use of isotopic analysis of vertebrae in reconstructing ontogenetic feeding ecology in white sharks. Ecology 87(4):829–834.  https://doi.org/10.1890/0012-9658(2006)87%5b829:UOIAOV%5d2.0.CO;2 CrossRefPubMedGoogle Scholar
  16. Estupiñán-Montaño C, Cedeño-Figueroa LG, Galván-Magaña F (2009) Feeding habits of the scalloped hammerhead shark Sphyrna lewini (Griffith & Smith, 1834) (Chondrichthyes) in the Ecuador Pacific. Rev Biol Mar Oceanogr 44(2):379–386.  https://doi.org/10.4067/S0718-19572009000200011 CrossRefGoogle Scholar
  17. Estupiñán-Montaño C, Cedeño-Figueroa LG, Estupiñán-Ortíz JF, Galván-Magaña F, Sandoval-Londoño A, Castañeda-Suárez D, Polo-Silva CJ (2018) Feeding habits and trophic level of the smooth hammerhead shark, Sphyrna zygaena (Carcharhiniformes: Sphyrnidae), off Ecuador. J Mar Biol Assoc UK 99(3):673–680.  https://doi.org/10.1017/S0025315418000474 CrossRefGoogle Scholar
  18. Farrell JW, Pedersen TF, Calvert SE, Nielsen B (1995) Glacial-interglacial changes in nutrient utilization in the equatorial Pacific Ocean. Nature 377:514–516CrossRefGoogle Scholar
  19. France RL (1993) Carbon-13 enrichment in benthic compared to planktonic algae: food web implications. Mar Ecol Prog Ser 124:307–312CrossRefGoogle Scholar
  20. Galván-Magaña F, Polo-Silva C, Hernández-Aguilar SB, Sandoval-Londoño A, Ochoa-Díaz MR, Aguilar-Castro N, Castañeda-Suárez D, Chavez-Costa A, Baigorrí-Santacruz A, Torres-Rojas YE, Abitia-Cárdenas L (2013) Shark predation on cephalopods in the Mexican and Ecuadorian Pacific Ocean. Deep Sea Res Part II 95:52–62.  https://doi.org/10.1016/j.dsr2.2013.04.002 CrossRefGoogle Scholar
  21. Granger J, Sigman DM, Lehmann MF, Tortell PD (2008) Nitrogen and oxygen isotope fractionation during dissimilatory nitrate reduction by denitrifying bacteria. Limnol Oceanogr 53(6):2533–2545.  https://doi.org/10.4319/lo.2008.53.6.2533 CrossRefGoogle Scholar
  22. Grubbs RD (2010) Ontogenetic shifts in movements and habitat use. In: Carrier JC, Musick JA, Heithaus MR (eds) Sharks and their relatives II: biodiversity, adaptive physiology, and conservation. Taylor & Francis Group, Boca Raton, pp 319–350CrossRefGoogle Scholar
  23. Harvey JT (1989) Food habits, seasonal abundance, size, and sex of the blue shark, Prionace glauca, in Monterey Bay, California. Calif Fish Game 75(1):33–44Google Scholar
  24. Hazen EL, Maxwell SM, Bailey H, Bograd SJ, Hamman M, Gaspar P, Godley BJ, Shillinger GL (2012) Ontogeny in marine tagging and tracking science: technologies and data gaps. Mar Ecol Prog Ser 457:221–240.  https://doi.org/10.3354/meps09857 CrossRefGoogle Scholar
  25. Hedges JI, Stern JH (1984) Carbon and nitrogen determinations of carbonate-containing solids. Limnol Oceanogr 29(3):657–663.  https://doi.org/10.4319/lo.1984.29.3.0657 CrossRefGoogle Scholar
  26. Heithaus MR, Vaudo JJ, Kreicker S, Layman CA, Krützen M, Burkholder DA, Gastrich K, Bessey C, Sarabia R, Cameron K (2013) Apparent resource partitioning and trophic structure of large-bodied marine predators in a relatively pristine seagrass ecosystem. Mar Ecol Prog Ser 481:225–237.  https://doi.org/10.3354/meps10235 CrossRefGoogle Scholar
  27. Hernández-Aguilar SB, Escobar-Sánchez O, Galván-Magaña F, Abitia-Cárdenas A (2016) Trophic ecology of the blue shark (Prionace glauca) based on stable isotopes (δ13C and δ15N) and stomach content. J Mar Biol Assoc UK 96(7):1403–1410.  https://doi.org/10.1017/S0025315415001393 CrossRefGoogle Scholar
  28. Heupel MR, Carlson JK, Simpfendorfer CA (2007) Shark nursery areas: concepts, definition, characterization and assumption. Mar Ecol Prog Ser 337:287–297.  https://doi.org/10.3354/meps337287 CrossRefGoogle Scholar
  29. Hussey NE, MacNeil M, Olin J, McMeans B, Kinney M, Chapman D, Fisk A (2012) Stable isotopes and elasmobranchs: tissue types, methods, applications and assumptions. J Fish Biol 80(5):1449–1484.  https://doi.org/10.1111/j.1095-8649.2012.03251.x CrossRefPubMedGoogle Scholar
  30. Hussey NE, MacNeil MA, Siple MC, Popp BN, Dubley SFJ, Fisk AT (2015) Expanded trophic complexity among large sharks. Food Webs 4(2015):1–7.  https://doi.org/10.1016/j.fooweb.2015.04.002 CrossRefGoogle Scholar
  31. 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(3):595–602.  https://doi.org/10.1111/j.1365-2656.2011.01806.x CrossRefGoogle Scholar
  32. Jereb P, Roper CFE (2010) Cephalopods of the world. An annotated and illustrated catalogue of cephalopod species known to date. Volume 2. Myopsid and Oegopsid squids. FAO Species catalogue for fishery purposes. No. 4, Vol. 2, RomeGoogle Scholar
  33. Juanes F, Buckel JA, Scharf FS (2001) Predatory behaviour and selective of a primary piscivore: comparison of this and non-fish prey. Mar Ecol Prog Ser 217:157–165.  https://doi.org/10.3354/meps217157 CrossRefGoogle Scholar
  34. Kim SL, Tinker MT, Estes JA, Koch PL (2012) Ontogenetic and among-individual variation in foraging strategies of northeast Pacific white sharks based on stable isotope analysis. PLoS One 7(9):e45068.  https://doi.org/10.1371/journal.pone.0045068 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Kiszka JJ, Charlot K, Hussey NE, Heithaus MR, Simon-Bouhet B, Humber F, Caurant F, Bustamante P (2014) Trophic ecology of common elasmobranchs exploited by artisanal shark fisheries off south-western Madagascar. Aquat Biol 23:29–38.  https://doi.org/10.3354/ab00602 CrossRefGoogle Scholar
  36. Koch PL (2007) Isotopic study of the biology of modern and fossil vertebrates. In: Michener R, Lajtha K (eds) Stable isotopes in ecology and environmental science, 2nd edn. Blackwell, Malden, pp 99–154CrossRefGoogle Scholar
  37. Kuboderea T, Watanabe H, Ichii T (2007) Feeding habits of the blue shark, Prionace glauca, and salmon shark, Lamna ditropis, in the transition region of the Western North Pacific. Rev Fish Biol Fish 17:111–124.  https://doi.org/10.1007/s11160-006-9020-z CrossRefGoogle Scholar
  38. Li Y, Gongo Y, Chen X, Dai X, Zhu J (2014) Trophic ecology of sharks in the Mid-East Pacific Ocean inferred from stable isotopes. J Ocean Univ China 13(2):278–282.  https://doi.org/10.1007/s11802-014-2071-1 CrossRefGoogle Scholar
  39. Li Y, Zhang Y, Dai X (2016) Trophic interactions among pelagic sharks and large predatory teleosts in the northeast central Pacific. J Exp Mar Biol Ecol 483(2016):97–103.  https://doi.org/10.1016/j.jembe.2016.04.013 CrossRefGoogle Scholar
  40. Loor-Andrade P, Pincay-Espinoza J, Rosas-Luis R (2017) Diet of the blue shark Prionace glauca in the Ecuadorian Pacific Ocean during the years 2013 to 2015. J Appl Ichthyol 33(3):558–562.  https://doi.org/10.1111/jai.13329 CrossRefGoogle Scholar
  41. López S, Meléndez R, Barría P (2010) Preliminary diet analysis of the blue shark Prionace glauca in the eastern South Pacific. Rev Biol Mar Oceanogr 45(S1):745–749.  https://doi.org/10.4067/S0718-19572010000400017 CrossRefGoogle Scholar
  42. López S, Barría P, Meléndez R (2012) Feeding and trophic relationships of two highly migratory sharks in the eastern south Pacific Ocean. Pan-Am J Aquat Sci 7(1):50–56Google Scholar
  43. Lowe CG, Wetherbee BM, Crow GL, Tester AL (1996) Ontogenetic dietary shifts and feeding behavior on the tiger shark, Galeocerdo cuvier, Hawaiian waters. Environ Biol Fish 47(2):203–211.  https://doi.org/10.1007/BF00005044 CrossRefGoogle Scholar
  44. Macko SA, Estep MLF (1984) Microbial alteration of stable nitrogen and carbon isotopic compositions of organic matter. Org Geochem 6:787–790.  https://doi.org/10.1016/0146-6380(84)90100-1 CrossRefGoogle Scholar
  45. MacNeil MA, Skomal GB, Fisk AT (2005) Stable isotopes from multiple tissues reveal diet switching in sharks. Mar Ecol Prog Ser 302:199–206.  https://doi.org/10.3354/meps302199 CrossRefGoogle Scholar
  46. Markaida U, Sosa-Nishizaki O (2010) Food and feeding habits of the blue shark Prionace glauca caught off Ensenada, Baja California, Mexico, with a review on its feeding. J Mar Biol Assoc UK 90(5):977–994.  https://doi.org/10.1017/s0025315409991597 CrossRefGoogle Scholar
  47. Martínez-Ortíz J, Galván-Magaña F, Carrera-Fernández M, Mendoza-Intriago D, Estupiñán-Montaño C, Cedeño-Figueroa L (2007) Abundancia estacional de tiburones desembarcados en Manta—Ecuador. In: Martínez-Ortíz J, Glaván-Magaña F (eds) Tiburones en el Ecuador: Casos de estudio/sharks in Ecuador: case studies. EPESPO-PMRC, Manta, pp 9–27Google Scholar
  48. Martínez-Ortíz J, Aires-da-Silva AM, Lennert-Cody CE, Maunder MN (2015) The Ecuadorian artisanal fishery for large pelagics: species composition and spatio-temporal dynamics. PLoS One 10(8):e0135136.  https://doi.org/10.1371/journal.pone.0135136 CrossRefPubMedPubMedCentralGoogle Scholar
  49. Maya-Meneses CI, Torres-Rojas YE, Galván-Magaña F, Aguiñiga-García S, Trasviña-Carrillo LD (2016) Trophic overlap between blue sharks (Prionace glauca) and shortfin makos (Isurus oxyrinchus): trophic linkages between two shark species in the Eastern Pacific Ocean food web. Food Web 7(2016):13–19.  https://doi.org/10.1016/j.fooweb.2016.03.002 CrossRefGoogle Scholar
  50. McCord ME, Campana SE (2003) A quantitative assessment of the diet of the blue shark (Prionace glauca) off Nova Scotia, Canada. J Northw Atl Fish Sci 32:57–63CrossRefGoogle Scholar
  51. McMeans B, Olin J, Benz G (2009) Stable isotope comparisons between embryos and mothers of a placentatrophic shark species. J Fish Biol 75(10):2464–2474.  https://doi.org/10.1111/j.1095-8649.2009.02402.x CrossRefPubMedGoogle Scholar
  52. Miller TW, Brodeur RD (2007) Diets of and trophic relationships among dominant marine nekton within the northern California current ecosystem. Fish Bull 105(4):548–559Google Scholar
  53. Nakano H (1994) Age, reproduction and migration of the blue shark in the North Pacific Ocean. Bull Natl Res Inst Far Seas Fish 31:141–256Google Scholar
  54. Newman SP, Handy RD, Gruber SH (2012) Ontogenetic diet shift and prey selection in nursery bound lemon sharks, Negaprion brevirostris, indicate a flexible foraging tactic. Environ Biol Fish 95(1):115–126.  https://doi.org/10.1007/s10641-011-9828-9 CrossRefGoogle Scholar
  55. Niño-Torres CA, Gallo-Reynoso JA, Galván-Magaña F, Escobar-Briones E, Macko SA (2006) Isotopic analysis of δ13C, δ15N, and δ34S “a feeding tale” in teeth of the longbeaked common dolphin, Delphinus capensis. Mar Mamm Sci 22(4):831–846.  https://doi.org/10.1111/j.1748-7692.2006.00065.x CrossRefGoogle Scholar
  56. Palacios DM (2002) Factor influencing the island-mass effect of the Galapagos Islands. Geophys Res Lett 29(23):49-1–49-4.  https://doi.org/10.1029/2002gl016232 CrossRefGoogle Scholar
  57. Palacios DM, Bograd SJ, Foley DG, Schwing FB (2006) Oceanographic characteristics of biological hot spots in the North Pacific: a remote sensing perspective. Deep Sea Res Part 2 53:250–569.  https://doi.org/10.1016/j.dsr2.2006.03.004 CrossRefGoogle Scholar
  58. Pardo-Gandarillas MC, Duarte F, Chong J, Ibáñez CM (2007) Dieta de tiburones juveniles Prionace glauca (Linnaeus, 1758) (Carcharhinidae: Carcharhiniformes) en la zona litoral centro-sur de Chile. Rev Biol Mar Oceanogr 42(3):365–369.  https://doi.org/10.4067/S0718-19572007000300015 CrossRefGoogle Scholar
  59. Peterson B, Fry B (1987) Stable isotopes in ecosystem studies. Ann Rev Ecol Syst 18:293–320CrossRefGoogle Scholar
  60. Polo-Silva CJ, Galván-Magaña F, Delgado-Huertas A (2012) Trophic inferences of the blue shark (Prionace glauca) in the Mexican Pacific from stable isotope analysis in teeth. Rapid Commun Mas Spectrom 26(4):1631–1638.  https://doi.org/10.1002/rcm.6275 CrossRefGoogle Scholar
  61. Polo-Silva C, Newsome SD, Galván-Magaña F, Grijalba-Bendeck M, Sanjuan-Muñoz A (2013) Trophic shift in the diet of the pelagic thresher shark based on stomach contents and stable isotope analyses. Mar Biol Res 9(10):958–971.  https://doi.org/10.1080/17451000.2013.793802 CrossRefGoogle Scholar
  62. Preti A, Soykan CU, Dewar H, Wells RJD, Spear N, Kohin S (2012) Comparative feeding ecology of shortfin mako, blue and thresher sharks in the California current. Environ Biol Fish 95(1):127–146.  https://doi.org/10.1007/s10641-012-9980-x CrossRefGoogle Scholar
  63. Revill AT, Young JW, Lansdell M (2009) Stable isotopic evidence for trophic groupings and bio-regionalization of predators and their prey in oceanic waters off Eastern Australia. Mar Biol 156(6):1241–1253.  https://doi.org/10.1007/s00227-009-1166-5 CrossRefGoogle Scholar
  64. Quezada-Romegialli C, Jackson AL, Harrod C (2018) tRophicPosition: Bayesian trophic position calculation with stable isotopes. R packages version 0.7.5. http://cran.r-project.org/web/packages/tRophicPsition
  65. R Development Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
  66. Rivera J, Hernández S, Galván F, Leonardo E (2015) A mockingbird Mimus polyglottos (Linnaeus, 1758) found in a stomach of a blue shark Prionace glauca (Linnaeus, 1758). Oceánides 30(2):53–54Google Scholar
  67. Rosas-Luis R, Navarro J, Loor-Andrade P, Forero MG (2017) Feeding ecology and trophic relationships of pelagic sharks and billfishes coexisting in the central eastern Pacific Ocean. Mar Ecol Prog Ser 573:191–201.  https://doi.org/10.3354/meps12186 CrossRefGoogle Scholar
  68. Vandeperre F, Aires-da-Silva A, Fontes J, Santos M, Serrão-Santos R, Afonso P (2014) Movements of blue sharks (Prionace glauca) across their life history. PLoS One 9(8):e.103538.  https://doi.org/10.1371/journal.pone.0103538 CrossRefGoogle Scholar
  69. Vander-Zanden, MJ, Rasmussen JB (1999) Primary consumer d15N and d13C and the trophic position of aquatic consumers. Ecology 80:1395–1404CrossRefGoogle Scholar
  70. Vaske-Júnior T, Rincón-Filho G (1998) Conteúdo estomacal dos tubarões azul (Prionace glauca) e anequim (Isurus oxyrinchus) em águas oceánicas no sul do Brasil. Rev Brasil Biol 58(3):445–452CrossRefGoogle Scholar
  71. Vaudo JJ, Matich P, Heithaus R (2010) Mother–offspring isotopes fractionation two species if placentatrophic sharks. J Fish Biol 77(7):1724–1727.  https://doi.org/10.1111/j.1095-8649.2010.02813.x CrossRefPubMedGoogle Scholar
  72. Young JW, Lansdell MJ, Campbell RA, Cooper SP, Juanes F, Guest MA (2010) Feeding ecology and niche segregation in oceanic top predators off Eastern Australia. Mar Biol 157(11):2347–2368.  https://doi.org/10.1007/s00227-010-1500-y CrossRefGoogle Scholar

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© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Fundación Alium PacificCaliColombia
  2. 2.Instituto Politécnico Nacional, Centro Interdisciplinario de Ciencias MarinasLa PazMexico
  3. 3.Instituto Andaluz de Ciencias de la Tierra (CSIC-UGR)GranadaSpain
  4. 4.Universidad San Francisco de Quito, Galápagos Science CenterIsla San CristóbalEcuador
  5. 5.Dirección del Parque Nacional Galápagos, Unidad Técnica Operativa San CristóbalIsla San CristóbalEcuador

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