Marine Biology

, 166:86 | Cite as

A genomic assessment of movement and gene flow around the South Florida vicariance zone in the migratory coastal blacknose shark, Carcharhinus acronotus

  • Pavel V. DimensEmail author
  • Stuart Willis
  • R. Dean Grubbs
  • David S. Portnoy
Original paper


South Florida has been identified as a genetic break for multiple mobile marine taxa but the mechanisms that impede gene flow largely remain unknown. To understand how South Florida functions as a barrier for blacknose shark, a highly migratory species that has genetically diverged Atlantic and Gulf populations, patterns of genetic variation were assessed in 212 individuals sampled from the Atlantic, eastern Gulf, and Florida Keys at 2213 nuclear-encoded SNP-containing loci. Results support divergence between the Gulf and Atlantic (FST ~ 0.002, P < 0.05), and 51 individuals caught in the Keys were assigned to the Gulf, as compared to only two individuals that assigned to the Atlantic, indicating that Florida Keys is largely composed of Gulf individuals. Further, two to three migrants were identified, all of which were Gulf individuals captured in the Atlantic. The results indicate that South Florida does not prevent individual movement between the Gulf and Atlantic and that the Keys may be a seasonal mixing zone. However, the Gulf and Atlantic remain genetically independent, suggesting that region-specific reproductive behavior/compatibility, or aspects of movement ecology, such as swimming energetics or temperature-driven interannual variability in migratory range, may maintain divergence rather than a physical barrier in South Florida.



We are thankful for tissue samples provided by A. Piercy (Florida Museum of Natural History, University of North Florida), J. Gelsleichter and R. Ford (University of North Florida), D. Bethea (NOAA Fisheries Panama City Laboratory), M. Drymon (Dauphin Island Sea Lab), W.B. Driggers, K. Hannan, C. Jones and L. Jones (NMFS, Mississippi Laboratories), B. Frazier and A. Shaw (SCDNR), C. Belcher (GADNR), C. Peterson and J. Imhoff (Florida State University). A debt of gratitude is owed to J. Puritz, C. M. Hollenbeck, and the rest of the Marine Genomics Laboratory for assistance and guidance with both laboratory practices and analyses. This article is publication number 22 of the Marine Genomics Laboratory at Texas A&M University-Corpus Christi, number 116 in the series Genetic Studies in Marine Fishes. Work was supported by the National Marine Fisheries Service under Saltonstall-Kennedy Grant No. NA10NMF4540080, the NOAA Fisheries - Gulf of Mexico Shark Pupping and Nursery program, NOAA Office of Protected Resources, Section – 6, the Guy Harvey Ocean Foundation, Texas Sea Grant College Program’s Grants-In-Aid of Graduate Research Program, and by funds through the College of Science and Engineering at Texas A&M University-Corpus Christi. Additionally, we thank Dr. Oscar Puebla and two anonymous reviewers for their time and helpful comments.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted. Field sample collections by FSU were approved under FSU IACUC protocols 1111 and 1411.

Supplementary material

227_2019_3533_MOESM1_ESM.html (28 kb)
Supplementary material 1 (HTML 27 kb)
227_2019_3533_MOESM2_ESM.pdf (119 kb)
Supplementary material 2 (PDF 119 kb)
227_2019_3533_MOESM3_ESM.pdf (220 kb)
Supplementary material 3 (PDF 220 kb)
227_2019_3533_MOESM4_ESM.pdf (228 kb)
Supplementary material 4 (PDF 227 kb)


  1. Baltazar-Soares M, Biastoch A, Harrod C et al (2014) Recruitment collapse and population structure of the European eel shaped by local ocean current dynamics. Curr Biol 24:104–108. CrossRefPubMedGoogle Scholar
  2. Begg GA, Friedland KD, Pearce JB (1999) Stock identification and its role in stock assessment and fisheries management: an overview. Fish Res 43:1–8. CrossRefGoogle Scholar
  3. Benavides MT, Horn RL, Feldheim KA et al (2011) Global phylogeography of the dusky shark Carcharhinus obscurus: implications for fisheries management and monitoring the shark fin trade. Endanger Species Res 14:13–22. CrossRefGoogle Scholar
  4. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Stat Soc Ser B (Methodol) 57:289–300. CrossRefGoogle Scholar
  5. Berg PR, Jentoft S, Star B, Ring KH, Knutsen H, Lien S, André C (2015) Adaptation to low salinity promotes genomic divergence in Atlantic Cod (Gadus morhua L.). Genome Biol Evol 7:1644–1663. CrossRefPubMedPubMedCentralGoogle Scholar
  6. Blanck A, Lamouroux N (2006) Large-scale intraspecific variation in life-history traits of European freshwater fish. J Biogeogr 34:862–875. CrossRefGoogle Scholar
  7. Bowen BW, Avise JC (1990) Genetic structure of Atlantic and Gulf of Mexico populations of sea bass, menhaden, and sturgeon: influence of zoogeographic factors and life-history patterns. Mar Biol 107:371–381. CrossRefGoogle Scholar
  8. Broughton RE, Gold JR (1997) Microsatellite development and survey of variation in northern bluefin tuna (Thunnus thynnus). Mol Mar Biol Biotech 6:308–314Google Scholar
  9. Burton RS (1986) Evolutionary consequences of restricted gene flow among natural populations of the copepod, Trigriopus californicus. BMS 39:526–535Google Scholar
  10. Carlson JK (2002) Shark nurseries in the northeastern Gulf of Mexico. Shark nursery grounds of the Gulf of Mexico and the East Coast waters of the United States: an overview. An internal report to NOAA’s Highly Migratory Species Office NOAA Fisheries Narragansett Lab 28:165–182Google Scholar
  11. Carlson JK, Palmer CL, Parsons GR (1999) Oxygen consumption rate and swimming efficiency of the Blacknose Shark, Carcharhinus acronotus.Copeia 1999:34. CrossRefGoogle Scholar
  12. Carlsson J, McDowell JR, Carlsson JEL, Graves JE (2006) Genetic identity of YOY bluefin tuna from the Eastern and Western Atlantic Spawning Areas. J Hered 98:23–28. CrossRefPubMedGoogle Scholar
  13. Castro JI (1993) The shark nursery of Bulls Bay, South Carolina, with a review of the shark nurseries of the southeastern coast of the United States. Environ Biol Fishes 38:37–48. CrossRefGoogle Scholar
  14. Castro JI (2010) The sharks of north America. Oxford University Press, OxfordGoogle Scholar
  15. Chapman DD, Feldheim KA, Papastamatiou YP, Hueter RE (2015) There and back again: a review of residency and return migrations in sharks, with implications for population structure and management. Ann Rev Mar Sci 7:547–570. CrossRefPubMedGoogle Scholar
  16. Clark E, Von Schmidt K (1965) Sharks of the central Gulf coast of Florida. BMS 15:13–83Google Scholar
  17. Conover DO (1992) Seasonality and the scheduling of life history at different latitudes. J Fish Biol 41:161–178. CrossRefGoogle Scholar
  18. Core Team R (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  19. Cornuet JM, Piry S, Luikart G et al (1999) New methods employing multilocus genotypes to select or exclude populations as origins of individuals. Genetics 153:1989–2000PubMedPubMedCentralGoogle Scholar
  20. Daly-Engel TS, Seraphin KD, Holland KN et al (2012) Global phylogeography with mixed-marker analysis reveals male-mediated dispersal in the endangered scalloped hammerhead shark (Sphyrna lewini). PLoS One 7:e29986. CrossRefPubMedPubMedCentralGoogle Scholar
  21. Dodrill JW (1977) A hook and line survey of the sharks found within five hundred meters of shore along Melbourne Beach, Brevard County, Florida. Doctoral dissertation, Florida Institute of TechnologyGoogle Scholar
  22. Driggers WB, Oakley D, Ulrich GF et al (2004) Reproductive biology of Carcharhinus acronotus in the coastal waters of South Carolina. J Fish Biol 64:1540–1551CrossRefGoogle Scholar
  23. Driggers WB, Ingram GJ, Grace MA, Carlson JK, Ulrich GF, Sulikowski JA, Quattro JM (2007) Life history and population genetics of blacknose sharks, Carcharhinus acronotus, in the South Atlantic Bight and the northern Gulf of Mexico. Southeast Data, Assessment & Review, Charleston, SCGoogle Scholar
  24. Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567. CrossRefPubMedGoogle Scholar
  25. Felder DL, Camp DK (2009) Gulf of Mexico origin, waters, and biota: biodiversity, volume I, 1st edn. Texas A&M University Press, College StationGoogle Scholar
  26. Foll M, Gaggiotti O (2008) A genome-scan method to identify selected loci appropriate for both dominant and codominant markers: a Bayesian perspective. Genetics 180:977–993. CrossRefPubMedPubMedCentralGoogle Scholar
  27. Gardiner JM, Whitney NM, Hueter RE (2015) Smells like home: the role of olfactory cues in the homing behavior of Blacktip Sharks, Carcharhinus limbatus. Integr Comp Biol 55:495–506. CrossRefPubMedGoogle Scholar
  28. GMFMC (2017) Amendment 26 to the fishery management plan for the coastal migratory pelagics fishery of the Gulf of Mexico and Atlantic Region. Gulf Marine Fisheries Manaement Council, TampaGoogle Scholar
  29. Gold JR, Richardson LR (1991) Genetic studies in marine fishes. IV. An analysis of population structure in the red drum (Sciaenops ocellatus) using mitochondrial DNA. Fish Res 12:213–241. CrossRefGoogle Scholar
  30. Gold JR, Richardson LR (1998) Population structure in greater amberjack, Seriola dumerili, from the Gulf of Mexico and the western Atlantic Ocean. Fish Bull 96:767–778Google Scholar
  31. Gold JR, Pak E, DeVries DA (2002) Population structure of king mackerel (Scomberomorus cavalla) around peninsular Florida, as revealed by microsatellite DNA. Fish Bull 100:491–509Google Scholar
  32. Grubbs RD, Musick JA, Conrath CL, Romine JG (2007) Long-term movements, migration, and temporal delineation of a summer nursery for juvenile sandbar sharks in the Chesapeake Bay region. Am Fish Soc Symp 50:87Google Scholar
  33. Han Z, Zheng W, Zhu W et al (2015) A barrier to gene flow in the Asian paddle crab, Charybdis japonica, in the Yellow Sea. ICES J Mar Sci 72:1440–1448. CrossRefGoogle Scholar
  34. Hauser L, Carvalho GR (2008) Paradigm shifts in marine fisheries genetics: ugly hypotheses slain by beautiful facts. Fish Fish 9:333–362. CrossRefGoogle Scholar
  35. Heithaus MR, Burkholder D, Hueter RE et al (2007) Spatial and temporal variation in shark communities of the lower Florida Keys and evidence for historical population declines. Can J Fish Aquat Sci 64:1302–1313. CrossRefGoogle Scholar
  36. Hendon JM, Higgs J, Sulikowski J (2014) A cooperative approach to updating and investigating anomalies in critical life history parameters of two exploited shark species, blacknose and finetooth sharks in the northern Gulf of Mexico. University of Southern Mississippi, Hattiesburg, p 31Google Scholar
  37. Hendry AP (2001) Adaptive divergence and the evolution of reproductive isolation in the wild: an empirical demonstration using introduced sockeye salmon. Genetica 112–113:515–534CrossRefGoogle Scholar
  38. Heupel MR, Simpfendorfer CA, Hueter RE (2004) Estimation of shark home ranges using passive monitoring techniques. Environ Biol Fish 71:135–142. CrossRefGoogle Scholar
  39. Hollenbeck CM, Portnoy DS, Gold JR (2018) Evolution of population structure in an estuarine-dependent marine fish. Ecol Evol 9(6):3141–3152CrossRefGoogle Scholar
  40. Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Resour 9:1322–1332. CrossRefPubMedPubMedCentralGoogle Scholar
  41. Hueter RE, Manire CA (1994) Bycatch and catch-release mortality of small sharks in the Gulf coast nursery grounds of Tampa Bay and Charlotte Harbor. Accessed 11 Feb 2019
  42. Hueter RE, Tyminski JP (2007) Species-specific distribution and habitat characteristics of shark nurseries in Gulf of Mexico waters off peninsular Florida and Texas. American Fisheries Society, New York, p 193Google Scholar
  43. Hueter RE, Heupel MR, Heist EJ, Keeney DB (2004) Evidence of philopatry in sharks and implications for the management of shark fisheries. J Northwest Atl Fish Sci 35:239–247. CrossRefGoogle Scholar
  44. Johnson MS, Black R (1982) Chaotic genetic patchiness in an intertidal limpet, Siphonaria sp. Mar Biol 70:157–164. CrossRefGoogle Scholar
  45. Jombart T, Devillard S, Balloux F (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet 11:94CrossRefGoogle Scholar
  46. Karl SA, Castro ALF, Lopez JA et al (2011) Phylogeography and conservation of the bull shark (Carcharhinus leucas) inferred from mitochondrial and microsatellite DNA. Conserv Genet 12:371–382. CrossRefGoogle Scholar
  47. Keeney DB, Heupel MR, Hueter RE, Heist EJ (2005) Microsatellite and mitochondrial DNA analyses of the genetic structure of blacktip shark (Carcharhinus limbatus) nurseries in the northwestern Atlantic, Gulf of Mexico, and Caribbean Sea. Mol Ecol 14:1911–1923. CrossRefPubMedGoogle Scholar
  48. Keller DB, Grubbs RD, Frazier B (2018) Philopatric migrations and intra-estuarine space use of the bonnethead, Sphyrna tiburo. In: 34th annual meeting of the American elasmobranch society and the 3rd quadrennial meeting of sharks international. Oral PresentationGoogle Scholar
  49. Kijewska A, Kalamarz-Kubiak H, Arciszewski B, Guellard T, Petereit C, Wenne R (2016) Adaptation to salinity in Atlantic cod from different regions of the Baltic Sea. J Exp Mar Biol Ecol 478:62–67. CrossRefGoogle Scholar
  50. Klimley AP (1987) The determinants of sexual segregation in the scalloped hammerhead shark, Sphyrna lewini. Environ Biol Fishes 18:27–40. CrossRefGoogle Scholar
  51. Klimley AP (1993) Highly directional swimming by scalloped hammerhead sharks, Sphyrna lewini, and subsurface irradiance, temperature, bathymetry, and geomagnetic field. Mar Biol 117:1–22. CrossRefGoogle Scholar
  52. Knip DM, Heupel MR, Simpfendorfer CA (2010) Sharks in nearshore environments: models, importance, and consequences. Mar Ecol Prog Ser 402:1–11. CrossRefGoogle Scholar
  53. Kohler NE, Turner PA (2007) Preliminary mark/recapture data for four species of small coastal sharks in the western North Atlantic. NOAA, NarragansettGoogle Scholar
  54. Lee TN, Rooth C, Williams E et al (1992) Influence of Florida Current, gyres and wind-driven circulation on transport of larvae and recruitment in the Florida Keys coral reefs. Cont Shelf Res 12:971–1002. CrossRefGoogle Scholar
  55. Lessios HA (1998) The first stage of speciation as seen in organisms separated by the Isthmus of Panama. In: Endless forms: species and speciation. Oxford University Press, New York, pp 186–201Google Scholar
  56. Lewontin RC (1974) The genetic basis of evolutionary change. Columbia University Press, New YorkGoogle Scholar
  57. Lynch-Stieglitz J, Curry WB, Slowey N (1999) Weaker Gulf stream in the Florida Straits during the last glacial maximum. Nature 402:644–648. CrossRefGoogle Scholar
  58. Mariani S, Hutchinson WF, Hatfield EMC et al (2005) North Sea herring population structure revealed by microsatellite analysis. Mar Ecol Prog Ser 303:245–257. CrossRefGoogle Scholar
  59. Marko PB (2002) Fossil calibration of molecular clocks and the divergence times of geminate species pairs separated by the isthmus of panama. Mol Biol Evol 19:2005–2021. CrossRefPubMedGoogle Scholar
  60. Marshall DJ, Monro K, Bode M, Keough MJ, Swearer S (2010) Phenotype-environment mismatches reduce connectivity in the sea. Ecol Lett 13:128–140. CrossRefPubMedGoogle Scholar
  61. McCandless CT, Kohler NE, Pratt HL (2007) Shark nursery grounds of the Gulf of Mexico and the East Coast waters of the United States. American Fisheries Society, Bethesda, MDGoogle Scholar
  62. McMillan LF, Fewster RM (2017) Visualizations for genetic assignment analyses using the saddlepoint approximation method. Biometrics 73:1029–1041. CrossRefPubMedGoogle Scholar
  63. Medved RJ, Marshall JA (1983) Short-term movements of young sandbar sharks, Carcharhinus plumbeus (Pisces, Carcharhinidae). BMS 33:87–93Google Scholar
  64. Meirmans PG, Van Tienderen PH (2004) genotype and genodive: two programs for the analysis of genetic diversity of asexual organisms. Mol Ecol Notes 4:792–794. CrossRefGoogle Scholar
  65. Mills LS, Allendorf FW (1996) The one-migrant-per-generation rule in conservation and management. Conserv Biol 10:1509–1518. CrossRefGoogle Scholar
  66. Musick JA (1999) Life in the slow lane: ecology and conservation of long-lived marine animals. American Fisheries Society, Hartford, CT, p 1Google Scholar
  67. Musick JA, Burgess G, Cailliet G et al (2000) Management of sharks and their relatives (elasmobranchii). Fisheries 25:9–13.;2 CrossRefGoogle Scholar
  68. Neigel JE (2009) Population genetics and biogeography of the Gulf of Mexico. Gulf of Mexico Origins, Waters Biota 1:1353–1369Google Scholar
  69. Nielsen EE, Nielsen PH, Meldrup D, Hansen MM (2004) Genetic population structure of turbot (Scophthalmus maximus L.) supports the presence of multiple hybrid zones for marine fishes in the transition zone between the Baltic Sea and the North Sea. Mol Ecol 13:585–595. CrossRefPubMedGoogle Scholar
  70. NMFS (2011a) SEDAR 21 Final Stock Assessment Report: HMS Gulf of Mexico Blacknose Shark. 415Google Scholar
  71. NMFS (2011b) SEDAR 21 Final Stock Assessment Report: HMS Atlantic Blacknose Shark. 438Google Scholar
  72. NMFS (2011c) SEDAR 21 Final Stock Assessment Report: HMS Atlantic Blacknose Shark. Southeast Data, Assessment, and Review, North Charleston, SCGoogle Scholar
  73. Paetkau D, Slade R, Burden M, Estoup A (2004) Genetic assignment methods for the direct, real-time estimation of migration rate: a simulation-based exploration of accuracy and power. Mol Ecol 13:55–65. CrossRefPubMedGoogle Scholar
  74. Palumbi SR (1994) Genetic divergence, reproductive isolation, and marine speciation. Annu Rev Ecol Syst 25:547–572. CrossRefGoogle Scholar
  75. Papastamatiou YP, Lowe CG, Caselle JE, Friedlander AM (2009) Scale-dependent effects of habitat on movements and path structure of reef sharks at a predator-dominated atoll. Ecology 90:996–1008. CrossRefPubMedGoogle Scholar
  76. Peterson BK, Weber JN, Kay EH et al (2012) Double digest RADseq: an inexpensive method for de novo SNP discovery and genotyping in model and non-model species. PLoS One 7:e37135. CrossRefPubMedPubMedCentralGoogle Scholar
  77. Piry S, Alapetite A, Cornuet JM et al (2004) GENECLASS2: a software for genetic assignment and first-generation migrant detection. J Hered 95:536–539. CrossRefPubMedGoogle Scholar
  78. Portnoy DS, Gold JR (2013) Finding geographic population structure in marine fish species with high gene flow. In: Proceedings of the 65th Gulf and Caribbean Fisheries Institute. Gulf and Caribbean Fisheries Institute, pp 384–389Google Scholar
  79. Portnoy DS, McDowell JR, Heist EJ et al (2010) World phylogeography and male-mediated gene flow in the sandbar shark, Carcharhinus plumbeus. Mol Ecol 19:1994–2010. CrossRefPubMedGoogle Scholar
  80. Portnoy DS, Hollenbeck CM, Belcher CN et al (2014) Contemporary population structure and post-glacial genetic demography in a migratory marine species, the blacknose shark, Carcharhinus acronotus. Mol Ecol 23:5480–5495. CrossRefPubMedGoogle Scholar
  81. Portnoy DS, Puritz JB, Hollenbeck CM et al (2015) Selection and sex-biased dispersal in a coastal shark: the influence of philopatry on adaptive variation. Mol Ecol 24:5877–5885. CrossRefPubMedGoogle Scholar
  82. Portnoy DS, Hollenbeck CM, Bethea DM et al (2016) Population structure, gene flow, and historical demography of a small coastal shark (Carcharhinus isodon) in US waters of the Western Atlantic Ocean. ICES J Mar Sci 73:2322–2332CrossRefGoogle Scholar
  83. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedPubMedCentralGoogle Scholar
  84. Quesada H, Beynon CM, Skibinski DO (1995) A mitochondrial DNA discontinuity in the mussel Mytilus galloprovincialis Lmk: pleistocene vicariance biogeography and secondary intergradation. Mol Biol Evol 12:521–524. CrossRefPubMedGoogle Scholar
  85. Rannala B, Mountain JL (1997) Detecting immigration by using multilocus genotypes. Proc Natl Acad Sci USA 94:9197–9201. CrossRefPubMedGoogle Scholar
  86. Riginos C, Cunningham CW (2005) Local adaptation and species segregation in two mussel (Mytilus edulis x Mytilus trossulus) hybrid zones. Mol Ecol 14:381–400. CrossRefPubMedGoogle Scholar
  87. Rocha LA, Craig MT, Bowen BW (2007) Phylogeography and the conservation of coral reef fishes. Coral Reefs 26:501–512. CrossRefGoogle Scholar
  88. Sandoval Laurrabaquio-A N, Islas-Villanueva V, Adams DH et al (2019) Genetic evidence for regional philopatry of the Bull Shark (Carcharhinus leucas), to nursery areas in estuaries of the Gulf of Mexico and western North Atlantic Ocean. Fish Res 209:67–74. CrossRefGoogle Scholar
  89. Sang TK, Chang HY, Chen CT, Hui CF (1994) Population structure of the Japanese eel, Anguilla japonica. Mol Biol Evol 11:250–260. CrossRefPubMedGoogle Scholar
  90. Schwartz FJ et al (1984) Occurrence, Abundance, and Biology of the Blacknose Shark, Carcharhinus acronotus, in North Carolina. negs. CrossRefGoogle Scholar
  91. SEDAR (2014) SEDAR 38, South Atlantic King mackerel Stock Assessment Report, p 502Google Scholar
  92. Seyoum S, McBride R, Puchutulegui C et al (2017) Genetic population structure of sheepshead, Archosargus probatocephalus (Sparidae), a coastal marine fish off the southeastern United States: multiple population clusters based on species-specific microsatellite markers. BMS 93:691–713. CrossRefGoogle Scholar
  93. Seyoum S, McBride RS, Tringali MD et al (2018) Genetic population structure of the spotted seatrout (Cynoscion nebulosus): simultaneous examination of the mtDNA control region and microsatellite marker results. BMS 94:47–71. CrossRefGoogle Scholar
  94. Shaklee JB, Bentzen P (1998) Genetic identification of stocks of marine fish and shellfish. BMS 62:589–621Google Scholar
  95. Sims DW, Quayle VA (1998) Selective foraging behaviour of basking sharks on zooplankton in a small-scale front. Nature 393:460–464. CrossRefGoogle Scholar
  96. Sotka EE, Wares JP, Barth JA et al (2004) Strong genetic clines and geographical variation in gene flow in the rocky intertidal barnacle Balanus glandula. Mol Ecol 13:2143–2156. CrossRefPubMedGoogle Scholar
  97. Springer S (1967) Social organization of shark population. In: Sharks, skate and rays. The John Hopkins Press, Baltimore, MD, pp 149–174Google Scholar
  98. Sulikowski JA, Driggers WB, Ford TS et al (2007) Reproductive cycle of the blacknose shark Carcharhinus acronotus in the Gulf of Mexico. J Fish Biol 70:428–440. CrossRefGoogle Scholar
  99. Svensson O, Gräns J, Celander MC, Havenhand J, Leder EH, Lindström K, Schöld S, van Oosterhout C, Kvarnemo C (2017) Immigrant reproductive dysfunction facilitates ecological speciation. Evo 71:2510–2521. CrossRefGoogle Scholar
  100. Tringali MD, Bert TM (1996) The genetic stock structure of common snook (Centropomus undecimalis). Can J Fish Aquat Sci 53:974–984. CrossRefGoogle Scholar
  101. Tsounis G, Rossi S, Gili J-M, Arntz W (2006) Population structure of an exploited benthic cnidarian: the case study of red coral (Corallium rubrum L.). Mar Biol 149:1059–1070. CrossRefGoogle Scholar
  102. Ulrich GF, Jones CM, Driggers WB, Drymon JM, Oakley D, Riley C (2007) Habitat utilization, relative abundance, and seasonality of sharks in the estuarine and nearshore waters of South Carolina. American Fisheries Society, New York, pp 125Google Scholar
  103. Vucetich JA, Waite TA (2000) Is one migrant per generation sufficient for the genetic management of fluctuating populations? Anim Conserv 3:261–266. CrossRefGoogle Scholar
  104. Walker BK (2009) Benthic Habitat Mapping of Miami-Dade County: Visual Interpretation of LADS Bathymetry and Aerial Photography. Florida, DEP report #RM069. Miami Beach, FL, p 47Google Scholar
  105. Wang J, Mooers CNK (1998) Three-dimensional perspectives of the Florida current: transport, potential vorticity, and related dynamical properties. Dyn Atmos Oceans 27:135–149. CrossRefGoogle Scholar
  106. Weersing K, Toonen RJ (2009) Population genetics, larval dispersal, and connectivity in marine systems. Mar Ecol Prog Ser 393:1–12. CrossRefGoogle Scholar
  107. Wetherbee BM, Rechisky EL (2000) Movement patterns of juvenile sandbar sharks on their nursery grounds in Delaware Bay. Biotelemetry 15:91–98Google Scholar

Copyright information

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

Authors and Affiliations

  1. 1.University of Southern Mississippi Gulf Coast Research LaboratoryOcean SpringsUSA
  2. 2.Institute for Biodiversity Science and SustainabilityCalifornia Academy of SciencesSan FranciscoUSA
  3. 3.Florida State University Coastal and Marine LaboratorySt. TeresaUSA
  4. 4.Texas A&M University, Corpus ChristiCorpus ChristiUSA

Personalised recommendations