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Environmental Biology of Fishes

, Volume 102, Issue 2, pp 267–283 | Cite as

Linking bonefish (Albula vulpes) populations to nearshore estuarine habitats using an otolith microchemistry approach

  • R. O. SantosEmail author
  • Rachael Schinbeckler
  • Natasha Viadero
  • M. F. Larkin
  • J. J. Rennert
  • J. M. Shenker
  • J. S. Rehage
Article

Abstract

Identifying the relative importance of various nursery areas is critical for understanding the ecological roles of diverse juvenile habitats, as well as for the sustainable management of fisheries and coastal resources. Recent field collections suggest that a portion of the bonefish (Albula vulpes) population in South Florida may be using nearshore estuarine habitats as nurseries. Nearshore marine habitats are traditionally considered nursery habitat for bonefish. However, the prevalence of their reliance on lower salinity areas is not known. To address this, we used otolith microchemistry using laser ablation inductively-coupled plasma mass spectrometry to examine variation in Strontium (Sr), a marker for salinity, and determine the connectivity between estuarine and marine habitats across the life of bonefish. Sr profiles from otoliths obtained in locations within South Florida (SFL, N = 40) and Southwest Cuba (SCB, N = 10) were compared using a juvenile-migration index (JMI), and change point models to assess the generality of a shift in salinity and thus habitats across life histories. Adult stages of bonefish otoliths collected in SFL and SCB locations showed Sr concentrations connected to marine, high-salinity environments. The JMI showed that a vast majority of individuals (68.4% and 70% in South Florida and Cuba, respectively) moved from low- to high-salinity environments between juvenile and adult stages. The change point models showed that these shifts to high salinity environments occurred suddenly (in 85% of those showing a low to high salinity change), and early in life (after 2 years in South Florida and after 4 years in Cuba) suggesting an ontogenetic habitat change. This study provided evidence that bonefish use low-salinity estuarine environments as juvenile habitats, perhaps more commonly than marine habitats. The reliance on low-salinity environments suggests the potential vulnerability of bonefish nearshore nursery habitats to disturbances associated with coastal freshwater discharges.

Keywords

Strontium Ontogenetic habitat shifts Florida Cuba Salinity environments 

Notes

Acknowledgments

We are grateful to the anglers, guides and our Cuban colleagues who assisted in the collection of samples. We would like to thank the International Forensic Research Institute at Florida International University for allowing the use of the Trace Evidence Analysis Facility. Funding was provided by Bonefish and Tarpon Trust and by an FIU Tropical Conservation Internship to R. Schinbeckler. The project was developed in collaboration with the FCE LTER program (NSF DEB-1237517). This is contribution #x from the Center for Coastal Oceans Research in the Institute of Water and Environment at Florida International University.

Supplementary material

10641_2018_839_MOESM1_ESM.docx (617 kb)
ESM 1 (DOCX 617 kb)

References

  1. Adams AJ (2017) Guidelines for evaluating the suitability of catch and release fisheries: lessons learned from Caribbean flats fisheries. Fish Res 186:672–680.  https://doi.org/10.1016/J.FISHRES.2016.09.027 CrossRefGoogle Scholar
  2. Adams AJ, Wolfe RK, Tringali MD et al (2007) Rethinking the status of Albula spp. Biology in the Caribbean and Western Atlantic. Biol Manag World Tarpon Bonefish Fish 203.  https://doi.org/10.1201/9781420004250.ch15
  3. Adams AJ, Horodysky AZ, Mcbride RS et al (2014) Global conservation status and research needs for tarpons (Megalopidae), ladyfishes (Elopidae) and bonefishes (Albulidae). Fish Fish 15:280–311.  https://doi.org/10.1111/faf.12017 CrossRefGoogle Scholar
  4. Albuquerque CQ, Miekeley N, Muelbert JH, Walther BD, Jaureguizar AJ (2012) Estuarine dependency in a marine fish evaluated with otolith chemistry. Mar Biol 159:2229–2239.  https://doi.org/10.1007/s00227-012-2007-5 CrossRefGoogle Scholar
  5. Ault JS (2008) Biology and management of the world tarpon and bonefish fisheries. CRC Press, Boca RatonGoogle Scholar
  6. Ault JS, Diaz GA, Smith SG, Luo J, Serafy JE (1999) An efficient sampling survey design to estimate pink shrimp population abundance in Biscayne Bay, Florida. North Am J Fish Manag 19:696–712.  https://doi.org/10.1577/1548-8675(1999)019<0696:AESSDT>2.0.CO;2 CrossRefGoogle Scholar
  7. Baisre JA, Arboleya Z (2006) Going against the flow: effects of river damming in Cuban fisheries. Fish Res 81:283–292.  https://doi.org/10.1016/J.FISHRES.2006.04.019 CrossRefGoogle Scholar
  8. Bath GE, Thorrold SR, Jones CM, Campana SE, McLaren JW, Lam JWH (2000) Strontium and barium uptake in aragonitic otoliths of marine fish. Geochim Cosmochim Acta 64:1705–1714.  https://doi.org/10.1016/S0016-7037(99)00419-6 CrossRefGoogle Scholar
  9. Beck MW, Heck KL Jr, Able KW et al (2001) The identification, conservation, and management of estuarine and marine nurseries for fish and invertebrates: a better understanding of the habitats that serve as nurseries for marine species and the factors that create site-specific variability in nurse. Bioscience 51:555–556.  https://doi.org/10.1641/0006-3568(2001)051 CrossRefGoogle Scholar
  10. Briceño HO, Boyer JN (2012) 2012 annual report of the water quality monitoring project for the water quality protection program of the Florida Keys National Marine Sanctuary. 1–79Google Scholar
  11. Browder JA, Ogden JC (1999) The natural South Florida system II: predrainage ecology. Urban Ecosyst 3:245–277.  https://doi.org/10.1023/A:1009504601357 CrossRefGoogle Scholar
  12. Browder JA, Alleman R, Markley S, Ortner P, Pitts PA (2005) Biscayne Bay conceptual ecological model. Wetlands 25:854–869. https://doi.org/10.1672/0277-5212(2005)025[0854:BBCEM]2.0.CO;2Google Scholar
  13. Brown RJ, Severin KP (2008) A preliminary otolith microchemical examination of the diadromous migrations of Atlantic tarpon Megalops atlanticus. Biol Manag World Tarpon Bonefish Fish Taylor Fr Group CRC Ser Mar Biol Boca Raton, Florida 259–274Google Scholar
  14. Brown RJ, Severin KP (2009) Otolith chemistry analyses indicate that water Sr:ca is the primary factor influencing otolith Sr:ca for freshwater and diadromous fish but not for marine fish. Can J Fish Aquat Sci 66:1790–1808.  https://doi.org/10.1139/F09-112 CrossRefGoogle Scholar
  15. Brownscombe JW, Danylchuk AJ, Adams AJ, Black B, Boucek R, Power M, Rehage JS, Santos RO, Fisher RW, Horn B, Haak CR, Morton S, Hunt J, Ahrens R, Allen MS, Shenker J, Cooke SJ (2018) Bonefish in South Florida: status, threats and research needs. Environ Biol Fish:1–20.  https://doi.org/10.1007/s10641-018-0820-5
  16. Campana S (1999) Chemistry and composition of fish otoliths:pathways, mechanisms and applications. Mar Ecol Prog Ser 188:263–297.  https://doi.org/10.3354/meps188263 CrossRefGoogle Scholar
  17. Canty A, Ripley B (2016) Boot: bootstrap R (S-plus) functionsGoogle Scholar
  18. Chen H, Shen K, Chang C, Iizuka Y, Tzeng WN (2008) Effects of water temperature, salinity and feeding regimes on metamorphosis, growth and otolith Sr:ca ratios of Megalops cyprinoides leptocephali. Aquat Biol 3:41–50.  https://doi.org/10.3354/ab00062 CrossRefGoogle Scholar
  19. Claro R, Lindeman KC (2003) Spawning aggregation sites of snapper and grouper species (Lutjanidae and Serranidae) on the insular shelf of Cuba. Gulf Caribb Res 14:91–106.  https://doi.org/10.18785/gcr.1402.07 CrossRefGoogle Scholar
  20. Claudet J, Osenberg CW, Domenici P, Badalamenti F, Milazzo M, Falcón JM, Bertocci I, Benedetti-Cecchi L, García-Charton JA, Goñi R, Borg JA, Forcada A, de Lucia GA, Pérez-Ruzafa Á, Afonso P, Brito A, Guala I, Diréach LL, Sanchez-Jerez P, Somerfield PJ, Planes S (2010) Marine reserves: fish life history and ecological traits matter. Ecol Appl 20:830–839.  https://doi.org/10.1890/08-2131.1 CrossRefGoogle Scholar
  21. Coates JH, Hovel KA (2014) Incorporating movement and reproductive asynchrony into a simulation model of fertilization success for a marine broadcast spawner. Ecol Model 283:8–18.  https://doi.org/10.1016/j.ecolmodel.2014.03.012 CrossRefGoogle Scholar
  22. Cowen RK, Paris CB, Srinivasan A (2006) Scaling of connectivity in marine populations. Science (80- ) 311:522–527.  https://doi.org/10.1126/science.1122039 CrossRefGoogle Scholar
  23. Crabtree RE, Harnden CW, Snodgrass D, Stevens C (1996) Age, growth, and mortality of bonefish, Albula vulpes, from the waters of the Florida keys. Fish Bull 94:442–451Google Scholar
  24. Davison A, Hinkley D (1997) Bootstrap methods and their applications. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  25. de la Guardia E, Giménez-Hurtado E, Defeo O et al (2018) Indicators of overfishing of snapper (Lutjanidae) populations on the southwest shelf of Cuba. Ocean Coast Manag 153:116–123.  https://doi.org/10.1016/j.ocecoaman.2017.12.006 CrossRefGoogle Scholar
  26. Doherty P, Fowler T (1994) An empirical test of recruitment limitation in a coral reef fish. Science 263:935–939.  https://doi.org/10.1126/science.263.5149.935 CrossRefGoogle Scholar
  27. Fablet R, Daverat F, De Pontual H (2007) Unsupervised Bayesian reconstruction of individual life histories from otolith signatures: case study of Sr:ca transects of European eel (Anguilla anguilla) otoliths. Can J Fish Aquat Sci 64:152–165.  https://doi.org/10.1139/f06-173 CrossRefGoogle Scholar
  28. Fourqurean J, Robblee M (1999) Florida bay: a history of recent ecological changes. Estuaries 22:345–357CrossRefGoogle Scholar
  29. Frezza PE, Clem SE (2015) Using local fishers’ knowledge to characterize historical trends in the Florida bay bonefish population and fishery. Environ Biol Fish 98:2187–2202.  https://doi.org/10.1007/s10641-015-0442-0 CrossRefGoogle Scholar
  30. Froeschke JT, Stunz GW (2012) Hierarchical and interactive habitat selection in response to abiotic and biotic factors: the effect of hypoxia on habitat selection of juvenile estuarine fishes. Environ Biol Fish 93:31–41.  https://doi.org/10.1007/s10641-011-9887-y CrossRefGoogle Scholar
  31. Gillanders BM, Able KW, Brown JA, Eggleston DB, Sheridan PF (2003) Evidence of connectivity between juvenile and adult habitats for mobile marine fauna: an important component of nurseries. Mar Ecol Prog Ser 247:281–295.  https://doi.org/10.3354/meps247281 CrossRefGoogle Scholar
  32. Goulart F, Galán ÁL, Nelson E, Soares-Filho B (2018) Conservation lessons from Cuba: connecting science and policy. Biol Conserv 217:280–288.  https://doi.org/10.1016/j.biocon.2017.10.033 CrossRefGoogle Scholar
  33. Grol MGG, Nagelkerken I, Rypel AL, Layman CA (2011) Simple ecological trade-offs give rise to emergent cross-ecosystem distributions of a coral reef fish. Oecologia 165:79–88.  https://doi.org/10.1007/s00442-010-1833-8 CrossRefGoogle Scholar
  34. Grol MGG, Rypel AL, Nagelkerken I (2014) Growth potential and predation risk drive ontogenetic shifts among nursery habitats in a coral reef fish. Mar Ecol Prog Ser 502:229–244.  https://doi.org/10.3354/meps10682 CrossRefGoogle Scholar
  35. Haak CR, Power M, Cowles GW, Danylchuk AJ (2018) Hydrodynamic and isotopic niche differentiation between juveniles of two sympatric cryptic bonefishes, Albula vulpes and Albula goreensis. Environ Biol Fish:1–17.  https://doi.org/10.1007/s10641-018-0810-7
  36. Hall MO, Furman BT, Merello M, Durako MJ (2016) Recurrence of Thalassia testudinum seagrass die-off in Florida bay, USA: initial observations. Mar Ecol Prog Ser 560:243–249.  https://doi.org/10.3354/meps11923 CrossRefGoogle Scholar
  37. Harnden CW, Crabtree RE, Shenker JM (1999) Onshore transport of elopomorph leptocephali and glass eels (Pisces: Osteichthyes) in the Florida keys. Gulf Mex Sci 17:17–26Google Scholar
  38. Hsieh C-H, Reiss CS, Hunter JR, Beddington JR, May RM, Sugihara G (2006) Fishing elevates variability in the abundance of exploited species. Nature 443:859–862.  https://doi.org/10.1038/nature05232 CrossRefGoogle Scholar
  39. Hussey NE, Kessel ST, Aarestrup K et al (2015) Aquatic animal telemetry: a panoramic window into the underwater world. Science 348:1255642.  https://doi.org/10.1126/science.1255642 CrossRefGoogle Scholar
  40. Izzo C, Reis-Santos P, Gillanders BM (2018) Otolith chemistry does not just reflect environmental conditions: a meta-analytic evaluation. Fish Fish 19:441–454.  https://doi.org/10.1111/faf.12264 CrossRefGoogle Scholar
  41. Kelble CR, Loomis DK, Lovelace S, Nuttle WK, Ortner PB, Fletcher P, Cook GS, Lorenz JJ, Boyer JN (2013) The EBM-DPSER conceptual model: integrating ecosystem services into the DPSIR framework. PLoS One 8:e70766.  https://doi.org/10.1371/journal.pone.0070766 CrossRefGoogle Scholar
  42. Klarenberg G, Ahrens R, Shaw S, Allen M (2018) Use of a dynamic population model to estimate mortality and recruitment trends for bonefish in Florida bay. Environ Biol Fish.  https://doi.org/10.1007/s10641-018-0805-4
  43. Lara MR, Jones DL, Chen Z, Lamkin JT, Jones CM (2007) Spatial variation of otolith elemental signatures among juvenile gray snapper (Lutjanus griseus) inhabiting southern Florida waters. Mar Biol 153:235–248.  https://doi.org/10.1007/s00227-007-0799-5 CrossRefGoogle Scholar
  44. Larkin MF (2011) Assessment of South Florida’ s bonefish stock. These Diss 214Google Scholar
  45. Larkin MF, Ault JS, Humston R, Luo J (2010) A mail survey to estimate the fishery dynamics of southern Florida’s bonefish charter fleet. Fish Manag Ecol 17:254–261.  https://doi.org/10.1111/j.1365-2400.2009.00718.x CrossRefGoogle Scholar
  46. Lauck T, Clark C, Mangel M, Munro G (1998) Implementing the precautionary principle in FIsheries management through marine reserves. Ecol Appl 8:72–78. https://doi.org/10.1890/1051-0761(1998)8[S72:ITPPIF]2.0.CO;2Google Scholar
  47. Layman CA, Silliman BR (2002) Preliminary survey and diet analysis of juvenile fishes of an estuarine creek on Andros Island, Bahamas. Bull Mar Sci 70:199–210Google Scholar
  48. Layman CA, Araujo 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.  https://doi.org/10.1111/j.1469-185X.2011.00208.x CrossRefGoogle Scholar
  49. Ligas A, Sartor P, Colloca F (2011) Trends in population dynamics and fishery of Parapenaeus longirostris and Nephrops norvegicus in the Tyrrhenian Sea (NW Mediterranean): the relative importance of fishery and environmental variables. Mar Ecol 32:25–35.  https://doi.org/10.1111/j.1439-0485.2011.00440.x CrossRefGoogle Scholar
  50. Lirman D, Deangelo G, Serafy J, Hazra A, Smith Hazra D, Herlan J, Luo J, Bellmund S, Wang J, Clausing R (2008) Seasonal changes in the abundance and distribution of submerged aquatic vegetation in a highly managed coastal lagoon. Hydrobiologia 596:105–120.  https://doi.org/10.1007/s10750-007-9061-x CrossRefGoogle Scholar
  51. Lirman D, Thyberg T, Santos R, Schopmeyer S, Drury C, Collado-Vides L, Bellmund S, Serafy J (2014) SAV communities of Western Biscayne Bay, Miami, Florida, USA: human and natural drivers of seagrass and macroalgae abundance and distribution along a continuous shoreline. Estuar Coasts 37:1243–1255.  https://doi.org/10.1007/s12237-014-9769-6 CrossRefGoogle Scholar
  52. Madden CJ, Rudnick DT, McDonald AA et al (2009) Ecological indicators for assessing and communicating seagrass status and trends in Florida Bay. Indic Everglades Restor 9:S68–S82.  https://doi.org/10.1016/j.ecolind.2009.02.004 Google Scholar
  53. Mateo I, Durbin EG, Appeldoorn RS, Adams AJ, Juanes F, Kingsley R, Swart P, Durant D (2010) Role of mangroves as nurseries for French grunt Haemulon flavolineatum and schoolmaster Lutjanus apodus assessed by otolith elemental fingerprints. Mar Ecol Prog Ser 402:197–212.  https://doi.org/10.3354/meps08445 CrossRefGoogle Scholar
  54. McGowan N, Fowler AM, Parkinson K, Bishop DP, Ganio K, Doble PA, Booth DJ, Hare DJ (2014) Beyond the transect: an alternative microchemical imaging method for fine scale analysis of trace elements in fish otoliths during early life. Sci Total Environ 494–495:177–186.  https://doi.org/10.1016/j.scitotenv.2014.05.115 CrossRefGoogle Scholar
  55. McManus MG, Travis J (1998) Effects of temperature and salinity on the life history of the sailfin molly (Pisces: Poeciliidae): lipid storage and reproductive allocation. Oecologia 114:317–325.  https://doi.org/10.1007/s004420050453 CrossRefGoogle Scholar
  56. Meynecke JO, Lee SY, Duke NC (2008) Linking spatial metrics and fish catch reveals the importance of coastal wetland connectivity to inshore fisheries in Queensland, Australia. 141:981–996.  https://doi.org/10.1016/j.biocon.2008.01.018
  57. Mojica R, Shenker JM, Harnden CW, Wagner DE (1995) Recruitment of bonefish, Albula vulpes, around Lee Stocking Island, Bahamas. Fish Bull 93:666–674Google Scholar
  58. Morat F, Letourneur Y, Dierking J, Pécheyran C, Bareille G, Blamart D, Harmelin-Vivien M (2014) The great melting pot common sole population connectivity assessed by otolith and water fingerprints. PLoS One 9.  https://doi.org/10.1371/journal.pone.0086585
  59. Mumby PJ, Edwards AJ, Ernesto Arias-González J, Lindeman KC, Blackwell PG, Gall A, Gorczynska MI, Harborne AR, Pescod CL, Renken H, C. C. Wabnitz C, Llewellyn G (2004) Mangroves enhance the biomass of coral reef fish communities in the Caribbean. Nature 427:533–536.  https://doi.org/10.1038/nature02286 CrossRefGoogle Scholar
  60. Murchie KJ, Cooke SJ, Danylchuk AJ, Danylchuk SE, Goldberg TL, Suski CD, Philipp DP (2013) Movement patterns of bonefish (Albula vulpes) in tidal creeks and coastal waters of Eleuthera, the Bahamas. Fish Res 147:404–412.  https://doi.org/10.1016/j.fishres.2013.03.019 CrossRefGoogle Scholar
  61. Nagelkerken I, Dorenbosch M, Verberk WCEP, Cocheret de la Morinière E, van der Velde G (2000) Importance of shallow-water biotopes of a Caribbean bay for juvenile coral reef fishes: patterns in biotope association, community structure and spatial distribution. Mar Ecol Prog Ser 202:175–192.  https://doi.org/10.3354/meps202175 CrossRefGoogle Scholar
  62. Nagelkerken I, Sheaves M, Baker R, Connolly RM (2015) The seascape nursery: a novel spatial approach to identify and manage nurseries for coastal marine fauna. Fish Fish 16:362–371.  https://doi.org/10.1111/faf.12057 CrossRefGoogle Scholar
  63. Nelson R (2002) Catch-and-release: a management toolfor Florida. In: Lucy J, Studholme AL (eds) Catch and Release in Marine Recreational Fisheries. American Fisheries Society, pp 11–14Google Scholar
  64. Olds AD, Connolly RM, Pitt KA, Maxwell PS (2012) Habitat connectivity improves reserve performance. Conserv Lett 5:56–63.  https://doi.org/10.1111/j.1755-263X.2011.00204.x CrossRefGoogle Scholar
  65. Olsen EM, Heino M, Lilly GR, Morgan MJ, Brattey J, Ernande B, Dieckmann U (2004) Maturation trends indicative of rapid evolution preceded the collapse of northern cod. Nature 428:932–935.  https://doi.org/10.1038/nature02430 CrossRefGoogle Scholar
  66. Orth RJ, Carruthers TJB, Dennison WC et al (2006) A global crisis for seagrass ecosystems. Bioscience 56:987–996. https://doi.org/10.1641/0006-3568(2006)56[987:agcfse]2.0.co;2Google Scholar
  67. Payne Wynne ML, Wilson KA, Limburg KE, Gillanders B (2015) Retrospective examination of habitat use by blueback herring (Alosa aestivalis) using otolith microchemical methods. Can J Fish Aquat Sci 72:1073–1086.  https://doi.org/10.1139/cjfas-2014-0206 CrossRefGoogle Scholar
  68. Perera Valderrama S, Hernández Ávila A, González Méndez J, Moreno Martínez O, Cobián Rojas D, Ferro Azcona H, Milián Hernández E, Caballero Aragón H, Alcolado PM, Pina Amargós F, Hernández González Z, Espinosa Pantoja L, Rodríguez Farrat LF (2017) Marine protected areas in Cuba. Bull Mar Sci.  https://doi.org/10.5343/bms.2016.1129
  69. Pinheiro J, Bates D, DebRoy S, Sarkar D (2017) nlme: Linear and nonlinear mixed effects models. R Dev Core Team 1–97Google Scholar
  70. Pittman SJ, Monaco ME, Friedlander AM, Legare B, Nemeth RS, Kendall MS, Poti M, Clark RD, Wedding LM, Caldow C (2014) Fish with chips: tracking reef fish movements to evaluate size and connectivity of Caribbean marine protected areas. PLoS One 9:e96028.  https://doi.org/10.1371/journal.pone.0096028 CrossRefGoogle Scholar
  71. R Core Team (2017) R: A language and environment for statistical computingGoogle Scholar
  72. Reis-Santos P, Gillanders BM, Tanner SE, Vasconcelos RP, Elsdon TS, Cabral HN (2012) Temporal variability in estuarine fish otolith elemental fingerprints: implications for connectivity assessments. Estuar Coast Shelf Sci 112:216–224.  https://doi.org/10.1016/j.ecss.2012.07.027 CrossRefGoogle Scholar
  73. Rohtla M, Vetemaa M (2016) Otolith chemistry chimes in: migratory environmental histories of Atlantic tarpon (Megalops atlanticus) caught from offshore waters of French Guiana. Environ Biol Fish 99:593–602.  https://doi.org/10.1007/s10641-016-0501-1 CrossRefGoogle Scholar
  74. Rooker JR, Kraus RT, Secor DH (2004) Dispersive behaviors of black drum and red drum: is otolith Sr:ca a reliable indicator of salinity history? Estuaries 27:334–341.  https://doi.org/10.1007/BF02803389 CrossRefGoogle Scholar
  75. Ross G (2015) Parametric and nonparametric sequential change detection in R: The cpm package. J Stat Softw 66:forthcoming.  https://doi.org/10.18637/jss.v066.i03
  76. Rudnick DT, Ortner PB, Browder JA, Davis SM (2005) A conceptual ecological model of Florida Bay. Wetlands 25:870–883. https://doi.org/10.1672/0277-5212(2005)025[0870:ACEMOF]2.0.CO;2Google Scholar
  77. Santos RO, Lirman D, Serafy JE (2011) Quantifying freshwater-induced fragmentation of submerged aquatic vegetation communities using a multi-scale landscape ecology approach. Mar Ecol Prog Ser 427:233–246.  https://doi.org/10.3354/meps08996 CrossRefGoogle Scholar
  78. Santos RO, Lirman D, Pittman SJ (2015) Long-term spatial dynamics in vegetated seascapes: fragmentation and habitat loss in a human-impacted subtropical lagoon. Mar Ecol 37:200–214.  https://doi.org/10.1111/maec.12259 CrossRefGoogle Scholar
  79. Santos RO, Rehage JS, Adams AJ, Black BD, Osborne J, Kroloff EKN (2017) Quantitative assessment of a data-limited recreational bonefish fishery using a time-series of fishing guides reports. 12:e0184776.  https://doi.org/10.1371/journal.pone.0184776
  80. Santos RO, Lirman D, Pittman SJ, Serafy JE (2018) Spatial patterns of seagrasses and salinity regimes interact to structure marine faunal assemblages in a subtropical bay. Mar Ecol Prog Ser 594:21–38.  https://doi.org/10.3354/meps12499 CrossRefGoogle Scholar
  81. Schilling H, Reis-Santos P, Hughes J, Smith JA, Everett JD, Stewart J, Gillanders BM, Suthers IM (2018) Evaluating estuarine nursery use and life history patterns of Pomatomus saltatrix in eastern Australia. Mar Ecol Prog Ser 598:187–199.  https://doi.org/10.3354/meps12495 CrossRefGoogle Scholar
  82. Seeley M, Miller N, Walther B (2015) High resolution profiles of elements in Atlantic tarpon (Megalops atlanticus) scales obtained via cross-sectioning and laser ablation ICP-MS: a literature survey and novel approach for scale analyses. Environ Biol Fish 98:2223–2238.  https://doi.org/10.1007/s10641-015-0443-z CrossRefGoogle Scholar
  83. Selkoe KA, Henzler CM, Gaines SD (2008) Seascape genetics and the spatial ecology of marine populations. Fish Fish 9:363–377.  https://doi.org/10.1111/j.1467-2979.2008.00300.x CrossRefGoogle Scholar
  84. Stabenau E, Kotun K (2012) Salinity and hydrology of Florida bay: status and trends 1990-2009Google Scholar
  85. Stanley RRE, Bradbury IR, DiBacco C, Snelgrove PVR, Thorrold SR, Killen SS (2015) Environmentally mediated trends in otolith composition of juvenile Atlantic cod (Gadus morhua). ICES J Mar Sci J du Cons 72:2350–2363.  https://doi.org/10.1093/icesjms/fsv070 CrossRefGoogle Scholar
  86. Sturrock AM, Hunter E, Milton JA, EIMF, Johnson RC, Waring CP, Trueman CN (2015) Quantifying physiological influences on otolith microchemistry. Methods Ecol Evol 6:806–816.  https://doi.org/10.1111/2041-210X.12381 CrossRefGoogle Scholar
  87. Tabouret H, Lord C, Bareille G, Pécheyran C, Monti D, Keith P (2011) Otolith microchemistry in Sicydium punctatum: indices of environmental condition changes after recruitment. Aquat Living Resour 24:369–378.  https://doi.org/10.1051/alr/2011137 CrossRefGoogle Scholar
  88. Wallace EM, Tringali MD (2010) Identification of a novel member in the family Albulidae (bonefishes). J Fish Biol 76:1972–1983.  https://doi.org/10.1111/j.1095-8649.2010.02639.x CrossRefGoogle Scholar
  89. Webb SD, Woodcock SH, Gillanders BM (2012) Sources of otolith barium and strontium in estuarine fish and the influence of salinity and temperature. Mar Ecol Prog Ser 453:189–199.  https://doi.org/10.3354/meps09653 CrossRefGoogle Scholar
  90. Yeager LA, Acevedo C, Layman CA (2012) Effects of seascape context on condition, abundance, and secondary production of a coral reef fish, Haemulon plumierii. Mar Ecol Prog Ser 462:231–240.  https://doi.org/10.3354/meps09855 CrossRefGoogle Scholar
  91. Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer-Verlag, New YorkCrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • R. O. Santos
    • 1
    Email author
  • Rachael Schinbeckler
    • 2
  • Natasha Viadero
    • 1
  • M. F. Larkin
    • 3
  • J. J. Rennert
    • 4
  • J. M. Shenker
    • 4
  • J. S. Rehage
    • 1
  1. 1.Earth and Environment DepartmentFlorida International UniversityMiamiUSA
  2. 2.Marine Biology, Department of Biological SciencesFlorida International UniversityMiamiUSA
  3. 3.National Oceanic and Atmospheric Administration, Southeast Regional OfficeSt. PetersburgUSA
  4. 4.Biology DepartmentFlorida Institute of TechnologyMelbourneUSA

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