Marine Biodiversity

, Volume 47, Issue 1, pp 37–53 | Cite as

Morphological and genetic species diversity in ostracods (Crustacea: Oligostraca) from Caribbean reefs

  • Alexandra M. Galindo Estronza
  • Mónica Alfaro
  • Nikolaos V. Schizas
Caribbean Coral Reefs

Abstract

The taxonomy and ecology of ostracods in the Caribbean remain incomplete, even though they are among the most successful and ubiquitous microcrustaceans of marine ecosystems. In an effort to enhance our knowledge of the biodiversity, abundance, and distribution of benthic ostracods, several sediment samples were collected from mesophotic coral ecosystems (MCEs) of Puerto Rico and U.S. Virgin Islands at different depths (30–102 m) using technical diving. The highest densities of ostracods were found in the deepest samples (≥61 m), and these were the most abundant and diverse assemblages. All ostracods collected belong to the subclasses Myodocopa Sars and Podocopa Sars. Myodocopa was represented by the families Cypridinidae Baird, Polycopidae Sars, Sarsiellidae Brady & Norman, Rutidermatidae Brady & Norman, Cylindroleberididae Müller, and Philomedidae Müller. On the other hand, Podocopa was represented by the following families: Bairdiidae Sars, Pontocyprididae Müller, Candonidae Kaufmann (subfamily Paracypridinae Sars), Macrocyprididae Müller, Loxoconchidae Sars, Xestoleberididae Sars, Cytherellidae Sars and Cytheromatidae Elofson. The subclass Podocopa showed the highest number of individuals and species. There was a ~100 % correspondence between morphologically identified species and genetically defined species through a short region of the nuclear large subunit ribosomal DNA, which was shown to be appropriate for species recognition and discrimination in ostracods. Using a morphological (shell shape and ornamentation) and molecular barcoding approach (28S rDNA), we provide the first report of the biodiversity of ostracods in the mesophotic coral ecosystems of northeastern Caribbean.

Keywords

Ostracoda Mesophotic coral ecosystems Morphology Molecular Barcoding Caribbean Puerto Rico U.S. Virgin Islands 

Notes

Acknowledgments

We thank the Technical Diving Team of the Department of Marine Sciences: Ivonne Bejarano, Milton Carlo, Michael Nemeth, Hector Ruiz, and Clark Sherman, for the collection of mesophotic samples. Undergraduate students from the Department of Biology assisted with the processing of samples. We are thankful to Dr. Todd Oakley and his laboratory crew (University of California Santa Barbara), Dr. Simone Nunes (Universidade Federal do Rio Grande do Norte), and María Inés F. Ramos (Museu Goeldi) for looking at some Ostracoda confocal pictures and helping with family designations. The 2010–2012 Mesophotic Cruises were supported by NOAA awards to the Caribbean Coral Reef Institute (CCRI) of UPRM: NA06NOS4780190, NA10NOS4260223, NA11NOS4260157, and NA11NOS4260184. Sea Grant of Puerto Rico awarded to NVS and MA, funded partially this project. The first author was supported by the Lerner Gray Memorial Fund of the American Museum of Natural History, International Women’s Fishing Association (IWFA), Sigma Xi Grants-In-Aid of Research (Grant ID: G20130315164016), Golden Key International Honour Society (Research Grant), and HHMI (Howard Hughes Medical Institute). We thank the CCRI and Dr. Richard Appeldoorn (UPRM) for providing a research assistantship to the first author during a portion of the study. We are also grateful for the constructive comments and suggestions provided by the anonymous reviewers on earlier versions of the manuscript.

Supplementary material

12526_2016_525_MOESM1_ESM.pdf (116 kb)
Online Resource 1 GPS Coordinates, depth and date of sampling stations from MCEs of Puerto Rico (PR) and U.S. Virgin Islands (USVI) (PDF 115 kb)
12526_2016_525_MOESM2_ESM.pdf (104 kb)
Online Resource 2 Coordinates, depth and date of sampling stations from shallow-water habitats of Puerto Rico (PR), U.S. Virgin Islands (USVI) and other areas of the Caribbean, North Atlantic and Pacific (PDF 103 kb)
12526_2016_525_MOESM3_ESM.pdf (137 kb)
Online Resource 3 Species and Morphbank images accession numbers used in this study. Numbers after species name signify sample identifiers. (PDF 136 kb)
12526_2016_525_MOESM4_ESM.pdf (121 kb)
Online Resource 4 Sequence alignment of 28S (v-x) and (dd-ff) regions for the studied Myodocopa and Podocopa species. Sequences were aligned with MUSCLE (Edgar 2004) as implemented in MEGA 7 (Kumar et al. 2016) (PDF 120 kb)

References

  1. Alvarez CA, Blackwelder PL, Hood T, Nelsen TA, Featherstone C (2000) Ostracods as indicators of natural and anthropogenically-induced changes in coastal marine environments. Proc 17th Int Conf Coast Soc 896–905Google Scholar
  2. Appeldoorn R, Ballantine D, Bejarano I, Carlo M, Nemeth M, Otero E, Pagan F, Ruiz H, Schizas NV, Sherman C, Weil E (2015) Mesophotic coral ecosystems and impacts from anthropogenic stress: a case study at Ponce, Puerto Rico. Coral Reefs 1–13Google Scholar
  3. Baker JH, Hulings NC (1966) Recent marine ostracod assemblages of Puerto Rico. Inst Mar Sci (Texas) 11:108–125Google Scholar
  4. Benson RH (1959) Ecology of recent ostracodes of the Todos Santos Bay region, Baja California, Mexico. Univ Kans Paleontol Contrib 23:1–80Google Scholar
  5. Benson RH, Coleman GL (1963) Recent marine Ostracoda from the eastern Gulf of Mexico. Univ Kans Paleontol Contrib Arthropod Article 2:1–52Google Scholar
  6. Bongaerts P, Ridgway T, Sampayo EM, Hoegh-Guldberg O (2010) Assessing the “deep reef refugia” hypothesis: focus on Caribbean Reefs. Coral Reefs 29:309–327CrossRefGoogle Scholar
  7. Brady GS (1880) Report of the ostracoda dredged by the H.M.S. Challenger during the years 1873–1876. Report on the scientific results of the voyage of H.M.S. Challenge Zool 1:1–184Google Scholar
  8. Bucklin A, Steinke D, Blanco-Bercial L (2011) DNA barcoding of marine metazoa. Ann Rev Mar Sci 3:471–508CrossRefPubMedGoogle Scholar
  9. Cohen AC (1982) Ostracoda. In: Parker S (ed) Synopsis and classification of living organisms. McGraw-Hill Book Company, Inc., New York, pp 181–202Google Scholar
  10. Cohen AC, Peterson DE, Maddocks RF (2007) Ostracoda. In: Carlton JT (ed) The Light & Smith Manual: intertidal invertebrates from Central California to Oregon, 4th edn. University of California Press, Berkeley, pp 417–446Google Scholar
  11. Corgosinho PHC, Schizas NV (2013) Archeolourinia shermani, a new genus and species of Louriniidae (Copepoda: Harpacticoida) from a Caribbean mesophotic zone. J Mar Biol Assoc UK 93:651–657CrossRefGoogle Scholar
  12. Dasmahapatra KK, Elias M, Hill RI, Hoffman JI, Mallet J (2010) Mitochondrial DNA barcoding detects some species that are real, and some that are not. Mol Ecol Resour 10(2):264–273CrossRefPubMedGoogle Scholar
  13. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32(5):1792–1797CrossRefPubMedPubMedCentralGoogle Scholar
  14. Elofson O (1941) Zur Kenntnis der marinen Ostracoden Schwedens mit besonderer Berücksichtigung des Skageraks. Upps Univ Zool 19:215–534Google Scholar
  15. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39(4):783–791CrossRefGoogle Scholar
  16. Fricke H, Meischner D (1985) Depth limits of Bermudan scleractinian corals: a submersible survey. Mar Biol 88(2):175–187CrossRefGoogle Scholar
  17. García-Sais JR, Castro R, Sabater J, Carlo M (2001) Baseline characterization of coral reef and seagrass communities from Isla de Vieques, Puerto Rico. U.S. Coral Reef National Monitoring Program, NOAA, DNER 1–108Google Scholar
  18. García-Sais JR, Castro R, Sabater J, Carlo M (2004) Monitoring of coral reefs communities from Isla de Vieques, Puerto Rico. Report submitted to DNER, San Juan, pp 1–118Google Scholar
  19. García-Sais JR, Appeldoorn R, Battista T, Bauer L, Bruckner A, Caldow C, Carrubba L, Corredor J, Diaz E, Lilyestrom C, García-Moliner G, Hernández-Delgado E, Menza C, Morell J, Pait A, Sabater J, Weil E, Williams E, Williams S (2008) The state of coral reef ecosystems of the Commonwealth of Puerto Rico. In: Waddell J, Clarke A (eds) The state of coral reef ecosystems of the United States and Pacific Freely Associated States: 2008 NOAA Technical Memorandum NOS NCCOS 78. NOAA/NCCOS Center for Coastal Monitoring and Assessment’s Biogeography Team, Silver Spring, MD 75–116Google Scholar
  20. García-Sais JR, Sabater J, Esteves R, Capella J, Carlo M (2011) Characterization of benthic habitats and associated mesophotic reef communities at El Seco, southeast Vieques, Puerto Rico. Report submitted to the Caribbean Fishery Management Council, San Juan, pp 1–102Google Scholar
  21. Hajibabaei M, Janzen DH, Burns JM, Hallwachs W, Hebert PDN (2006) DNA barcodes distinguish species of tropical Lepidoptera. P Natl Acad Sci USA 103(4):968–971CrossRefGoogle Scholar
  22. Hajibabaei M, Singer GAC, Hebert PDN, Hickey DA (2007) DNA barcoding: how it complements taxonomy, molecular phylogenetics and population genetics. Trends Genet 23(4):167–172CrossRefPubMedGoogle Scholar
  23. Harrison-Nelson E, Kornicker LS (2007) Myodocopan Ostracoda (Crustacea) of the Gulf of Mexico. Gulf of Mexico: Origins, Waters, and Biota. Biodiversity, Texas A&M University Press 1:871–875Google Scholar
  24. Hebert PDN, Cywinska A, Ball SL, deWaard JR (2003) Biological identifications through DNA barcodes. P Roy Soc Lond B Biol 270(1512):313–321CrossRefGoogle Scholar
  25. Hebert PDN, Stoeckle MY, Zemlak TS, Francis CM (2004) Identification of birds through DNA barcodes. Plos Biol 2(10):1657–1663CrossRefGoogle Scholar
  26. Hickerson MJ, Meyer CP, Moritz C (2006) DNA barcoding will often fail to discover new animal species over broad parameter space. Syst Biol 55(5):729–739CrossRefPubMedGoogle Scholar
  27. Hillis DM, Dixon MT (1991) Ribosomal DNA: molecular evolution and phylogenetic inference. Q Rev Biol 66:411–453CrossRefPubMedGoogle Scholar
  28. Hinderstein LM, Marr JCA, Martínez FA, Dowgiallo MJ, Puglise KA, Pyle RL, Zawada DG, Appeldoorn R (2010) Introduction to mesophotic coral ecosystems: characterization, ecology, and management. Coral Reefs 29:247–251CrossRefGoogle Scholar
  29. Hiruta SF, Kobayashi N, Katoh T, Kajihara H (2016) Molecular phylogeny of cypridoid freshwater ostracods (Crustacea: Ostracoda), inferred from 18S and 28S rDNA sequences. Zool Sci 33(2):179–185CrossRefPubMedGoogle Scholar
  30. Hulings NC (1959) A comparison of the recent ostracod faunas of the Gulf of Mexico and the South Atlantic coast of the United States. In preprint of abstracts of papers of the International Oceanographic Congress: Washington, DC, American Association for the Advancement of Science 158–159Google Scholar
  31. Jarman SN, Nicol S, Elliott NG, McMinn A (2000) 28S rDNA evolution in the eumalacostraca and the phylogenetic position of krill. Mol Phylogenet Evol 17:26–36CrossRefPubMedGoogle Scholar
  32. Jessup ME (2014) Mesophotic coral ecosystems: tools and techniques for scientific exploration. In: Eckert G, Keller S, Tamone S (eds) Diving for Science 2014. Proc Am Acad Underwat Sci 33rd Symp 7–14Google Scholar
  33. Kahng E, Copus M, Wagner D (2014) Recent advances in the ecology of mesophotic coral ecosystems (MCEs). Curr Opin Environ Sustain 7:72–81CrossRefGoogle Scholar
  34. Karanovic I (2015) Barcoding of ancient Lake Ostracods (Crustacea) reveals cryptic speciation with extremely low distances. Plos One 10(3):1–17CrossRefGoogle Scholar
  35. Karanovic I, Orduña-Martínez L, Ardisson PL (2015) On the phylogenetic position of Pseudophilomedinae within Sarsielloidea (Ostracoda, Myodocopida), with a description of one new Harbansus from Ningaloo Reef and redescription of H. paucichelatus from Yucatan. Helgol Mar Res 69(1):37–56CrossRefGoogle Scholar
  36. Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16(2):111–120CrossRefPubMedGoogle Scholar
  37. Kornicker LS (1958) Ecology and taxonomy of recent marine ostracodes in the bimini Area, Great Bahama Bank. Publications of the Institute of Marine Science, University of Texas 5:194–30Google Scholar
  38. Kornicker LS (1961) Ecology and taxonomy of recent Bairdiinae (Ostracoda). Micropaleontology 7(1):55–70CrossRefGoogle Scholar
  39. Kornicker LS (1979) Ostracoda. In: Fairbridge RW, Jablonski D (eds) The encyclopedia of paleontology. Dowden, Hutchinson and Ross, Inc, Stroudsburg, pp 499–504CrossRefGoogle Scholar
  40. Kornicker LS (1981) Revision, distribution, ecology, and ontogeny of the ostracode subfamily cyclasteropinae (Myodocopina: Cylindroleberididae). Smithsonian Contributions to Zoology 319:1–548Google Scholar
  41. Kornicker LS (1983) Rutidermatidae of the continental shelf of Southeastern North America and the Gulf of Mexico (Ostracoda: Myodocopina). Smithsonian Contributions to Zoology 371:1–86Google Scholar
  42. Kornicker LS (1984a) Philomedidae of the continental shelf of Eastern North America and the Northern Gulf of Mexico (Ostracoda: Myodocopina). Smithsonian Contributions to Zoology 393:1–78Google Scholar
  43. Kornicker LS (1984b) Cypridinidae of the continental shelves of Southeastern North America, the Northern Gulf of Mexico, and the West Indies (Ostracoda: Myodocopina). Smithsonian Contributions to Zoology 401:1–37Google Scholar
  44. Kornicker LS (1986a) Cylindroleberididae of the Western North Atlantic and Northern Gulf of Mexico, and Zoogeography of the Myodocopina (Ostracoda). Smithsonian Contributions to Zoology 425:1–139Google Scholar
  45. Kornicker LS (1986b) Sarsiellidae of the Western Atlantic and Northern Gulf of Mexico, and revision of the Sarsiellinae (Ostracoda: Myodocopina). Smithsonian Contributions to Zoology 415:1–217Google Scholar
  46. Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol (accepted)Google Scholar
  47. Lesser MP, Slattery M, Leichter JJ (2009) Ecology of mesophotic coral reefs. J Exp Mar Biol Ecol 375:1–8CrossRefGoogle Scholar
  48. Littler MM, Littler DS, Hanisak MD (1991) Deepwater rhodolith distribution, productivity, and growth history at sites of formation and subsequent degradation. J Exp Mar Biol Ecol 150:163–182CrossRefGoogle Scholar
  49. Locker SD, Armstrong RA, Battista TA, Rooney J, Sherman C, Zawada DG (2010) Geomorphology of mesophotic coral ecosystems. Coral Reefs 29:329–345CrossRefGoogle Scholar
  50. Lum KE, Syme AE, Schwab AK, Oakley TH (2008) Euphilomedes chupacabra (Ostracoda: Myodocopida: Philomedidae), a new demersal marine species from coastal Puerto Rico with male-biased vespertine swimming activity. Zootaxa 1684:35–57Google Scholar
  51. Machain ML (1996) Inventario y Catálogo de Ostrácodos Recientes de los Mares Mexicanos. Universidad Nacional Autónoma de México, Instituto de Ciencias del Mar y Limnología, Informe final SNIB-CONABIO. Proyecto No. B027. México, D.F. 1–46Google Scholar
  52. Machida RJ, Knowlton N (2012) PCR primers for metazoan nuclear 18S and 28S ribosomal DNA sequences. Plos One 7(9):1–11Google Scholar
  53. Maddocks RF (1969) Revision of recent Bairdiidae (Ostracoda). Bull US Natl Mus 295:1–126CrossRefGoogle Scholar
  54. Maddocks RF (1974) Ostracodes. In: Bright TS, Pequegnat LH (eds) Biota of the west flower garden bank. Gulf Publishing, Houston, pp 199–229Google Scholar
  55. Maddocks RF (1990) Living and fossil Macrocyprididae (Ostracoda). Univ Kans Paleontol Contrib Monogr 2:1–404Google Scholar
  56. Maddocks RF, Iliffe TM (1993) Thalassocypridine Ostracoda from anchialine habitats of Jamaica. J Crustac Biol 13:142–164CrossRefGoogle Scholar
  57. Maddocks RF, Machain-Castillo ML, Gío-Argáez FR (2007) Podocopan Ostracoda (Crustacea) of the Gulf of Mexico. Gulf of Mexico: Origins, Waters, and Biota. Biodiversity, Texas A&M University Press 1:877–894Google Scholar
  58. Martin-Rubio M, Elorza-Remón M, Rodriguez-Lazaro J, Pascual A (2006) Areal distribution and ecology of recent ostracods from the Joyel marsh (Cantabria, Spain). Geogaceta 40:187–190Google Scholar
  59. McIntyre AD (1969) Ecology of marine meiobenthos. Biol Rev 44(2):245–288CrossRefGoogle Scholar
  60. McKenzie KG (1971) Paradoxostoma pequegnati n. sp. (Ostracoda, Podocopina) from the Gulf of Mexico. Crustaceana 20:46–50CrossRefGoogle Scholar
  61. Morales-Núñez AG, Kornicker LS (2007) A new species of the genus Diasterope Kornicker, 1975 (Crustacea: Ostracoda: Cylindroleberididae) from Culebra Island, Puerto Rico. Proc Biol Soc Wash 120(3):271–278CrossRefGoogle Scholar
  62. Nagy ZT, Sonet G, Glaw F, Vences M (2012) First large-scale DNA barcoding assessment of reptiles in the biodiversity hotspot of Madagascar, based on newly designed COI primers. Plos One 7(3):1–11CrossRefGoogle Scholar
  63. Nichols JA (1979) A simple flotation technique for separating meiobenthic nematodes from fine-grained sediments. Trans Am Microsc Soc 98:127–130CrossRefGoogle Scholar
  64. Nigro LM, Angel MV, Blachowiak-Samolyk K, Hopcroft RR, Bucklin A (2016) Identification, discrimination, and discovery of species of marine planktonic ostracods using DNA barcodes. Plos One 11(1):1–17CrossRefGoogle Scholar
  65. Oakley TH, Cunningham CW (2002) Molecular phylogenetic evidence for the independent evolutionary origin of an arthropod compound eye. Proc Natl Acad Sci 99(3):1426–1430CrossRefPubMedPubMedCentralGoogle Scholar
  66. Oakley TH, Wolfe JM, Lindgren AR, Zaharoff AK (2012) Phylotranscriptomics to bring the understudied into the fold: monophyletic ostracoda, fossil placement, and pancrustacean phylogeny. Mol Biol Evol 30(1):215–233CrossRefPubMedGoogle Scholar
  67. Ogoh K, Ohmiya Y (2004) Complete mitochondrial DNA sequence of the sea-firefly, Vargula hilgendorfii (Ostracoda, Crustacea) with duplicate control regions. Gene 327:131–139CrossRefPubMedGoogle Scholar
  68. Palacios-Fest MR, Gío Argáez FR (1979) Sobre la presencia de dos especies de Havanardia Pokorny, 1968 (Bairdiidae, Ostracoda, Crustacea) en el Caribe Mexicano. Univ Nac Autón Méx, Inst Geol Rev 3:24–28Google Scholar
  69. Palacios-Fest MR, Gío Argáez FR, Krutak PR (1983) Los ostrácodos (Crustacea) recientes del Caribe Mexicano y su significación faunística. Univ Nac Autón Méx, An Inst Cienc Mar Limnología 10:195–208Google Scholar
  70. Petrescu I, Chatterjee T, Schizas NV (2012) New genus and new species of Cumaceans (Crustacea: Peracarida: Cumacea) from the mesophotic coral ecosystem of SW Puerto Rico, Caribbean Sea. Zootaxa 3476:55–61Google Scholar
  71. Petrescu I, Chatterjee T, Schizas NV (2013) Two new species of the genus Cumella (Crustacea: Cumacea: Nannastacidae) associated with mesophotic reefs of Puerto Rico and St. Croix, Caribbean Sea. Cah Biol Mar 54:257–262Google Scholar
  72. Petrescu, I, Chatterjee T, Schizas NV (2016). New species and new records of Cumacea (Crustacea: Peracarida: Cumacea) from mesophotic reefs of Puerto Rico and US Virgin Islands, Caribbean Sea. Zootaxa (Accepted)Google Scholar
  73. Puri HS, Hulings NC (1957) Recent ostracode facies from Panama City to Florida Bay area. Gulf Coast Assoc Geol Soc Trans 7:167–190Google Scholar
  74. Remane HC (1933) Verteilung und Organisation der benthonischen Mikrofauna der Kieler Bucht. Wissenschaftliche Meeresuntersuchungen, Abt. Kieler 21:161–221Google Scholar
  75. Riegl B, Piller WE (2003) Possible refugia for reefs in time of environmental stress. Int J Earth Sci 92:520–531CrossRefGoogle Scholar
  76. Rivero-Calle S, Armstrong RA, Soto-Santiago FJ (2008) Biological and physical characteristics of a mesophotic coral reef: Black Jack reef, Vieques, Puerto Rico. Proceedings of the 11th International Coral Reef Symposium, Ft. Lauderdale, Florida, 7–11 July 2008. Session number 16Google Scholar
  77. Rodriguez-Lazaro J, Ruiz-Muñoz F (2012) A general introduction to ostracods: morphology, distribution, fossil record and applications. Dev Quat Sci 17:1–14Google Scholar
  78. Rubinoff D, Cameron S, Kipling W (2006) A genomic perspective on the shortcomings of mitochondrial DNA for “Barcoding” identification. J Hered 97(6):581–594CrossRefPubMedGoogle Scholar
  79. Ruiz F, González-Regalado ML, Borrego J (1994) Ostracods and pollution: the Odiel river estuary (Huelva, SO Spain). Coloquios de Paleontología, n. 46 Editorial Complutense, Madrid 175–189Google Scholar
  80. Ruppert EE, Fox RS, Barnes RD (2004) Crustacea. In: Rose N (ed) Invertebrate Zoology A Functional Evolutionary Approach, 7th edn. Brooks/Cole, Cengage Learning, Belmont, California 687–690Google Scholar
  81. Schizas NV, Dahms HU, Kangtia P, Corgosihno PHC, Galindo Estronza AM (2015) A new species of Longipedia Claus, 1863 (Copepoda: Harpacticoida: Longipediidae) from Caribbean mesophotic reefs with remarks on the phylogenetic affinities of Polyarthra. Mar Biol Res 11(8):789–803CrossRefGoogle Scholar
  82. Senna AR, Sorrentino R, Chatterjee T, Schizas NV (2014) A new species of Boca Lowry & Stoddart, 1997 (Amphipoda: Lysianassoidea: Aristiidae) from a mesophotic coral ecosystem off Puerto Rico, Caribbean Sea. Zootaxa 3884(5):429–436CrossRefPubMedGoogle Scholar
  83. Sherman C, Appeldoorn R, Carlo M, Nemeth M, Ruiz H, Bejarano I (2009) Use of technical diving to study deep reef environments in Puerto Rico. In: Pollock, N.W. (ed.), American Academy of Underwater Sciences 28th Scientific Symposium, Atlanta, Georgia, USA 58–65Google Scholar
  84. Sherman C, Nemeth M, Ruíz H, Bejarano I, Appeldoorn R, Pagán F, Schärer M, Weil E (2010) Geomorphology and benthic cover of mesophotic coral ecosystems of the upper insular slope of southwest Puerto Rico. Coral Reefs 29:347–360CrossRefGoogle Scholar
  85. Sherman C, Appeldoorn R, Ballantine D, Bejarano I, Carlo M, Kesling D, Nemeth M, Pagán F, Ruiz H, Schizas NV, Weil E (2013) Exploring the mesophotic zone: Diving operations and scientific highlights of three research cruises across Puerto Rico and US Virgin Islands. In Lang MA, Sayer MDJ, Proceedings of the 2013 AAUS/ESDP Curaçao Joint International Scientific Diving Symposium, October 24–27, 2013, Curaçao. Dauphin Island, AL: American Academy of Underwater Sciences 297–312Google Scholar
  86. Snelgrove PVR (1998) The biodiversity of marine macrofaunal organisms in marine sediments. Biodivers Conserv 7:1123–1132CrossRefGoogle Scholar
  87. Syme AE, Oakley TH (2012) Dispersal between shallow and abyssal seas and evolutionary loss and regain of compound eyes in cylindroleberidid ostracods: conflicting conclusions from different comparative methods. Syst Biol 61:314–336CrossRefPubMedGoogle Scholar
  88. Tinn O, Oakley TH (2008) Erratic rates of molecular evolution and incongruence of fossil and molecular divergence time estimates in Ostracoda (Crustacea). Mol Phylogenet Evol 48:157–167CrossRefPubMedGoogle Scholar
  89. Tressler WL (1954) Marine Ostracoda. Fish Bull Fish Wildl Serv U S 89:237–429Google Scholar
  90. Van den Bold WA (1974) Ornate Bairdiidae in the Caribbean. Geosci Man 6:29–40Google Scholar
  91. Van den Bold WA (1977) Distribution of marine podocopid Ostracoda in the Gulf of Mexico and the Caribbean. In Aspects of Ecology and Zoogeography of Recent and Fossil Ostracoda, ed. H. Löffler and D. Danielopol. Dr. W. Junk, The Hague 175–186Google Scholar
  92. Van den Bold WA (1988) Neogene paleontology in the northern Dominican Republic. 7: the subclass Ostracoda (Arthropoda: Crustacea). Bull Am Paleontol 94(329):1–105Google Scholar
  93. Vasconcelos R, Montero-Mendieta S, Simó-Riudalbas M, Sindaco R, Santos X, Fasola M, Llorente G, Razzetti E, Carranza S (2016) Unexpectedly high levels of cryptic diversity uncovered by a complete DNA barcoding of reptiles of the Socotra archipelago. Plos One 11(3):1–19Google Scholar
  94. Wakayama N, Abe K (2006) The evolutionary pathway of light emission in myodocopid Ostracoda. Biol J Linn Soc 87(3):449–455Google Scholar
  95. Yamaguchi S, Endo K (2003) Molecular phylogeny of Ostracoda (Crustacea) inferred from 18S ribosomal DNA sequences: implication for its origin and diversification. Mar Biol 143:23–38CrossRefGoogle Scholar

Copyright information

© Senckenberg Gesellschaft für Naturforschung and Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Alexandra M. Galindo Estronza
    • 1
    • 2
  • Mónica Alfaro
    • 1
  • Nikolaos V. Schizas
    • 2
  1. 1.Department of BiologyUniversity of Puerto Rico at MayagüezMayagüezUSA
  2. 2.Department of Marine SciencesUniversity of Puerto Rico at MayagüezMayagüezUSA

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