Morphological recognition of cryptic species in the planktonic foraminifer Orbulina universa

Marine Micropaleontology

Volumn 71, Issue 3-4, 2009, Pages 148-165

  Morard, Raphaël ^a   Quillévéré, Frédéric ^a   Escarguel, Gilles ^a   Ujiie, Yurika ^b   de Garidel Thoron, Thibault ^c   Norris, Richard D ^d   de Vargas, Colomban ^b  

^a UNIVERSITÉ LYON 1   (France)

^b STATION BIOLOGIQUE DE ROSCOFF   (France)

^c AIX MARSEILLE UNIVERSITY   (France)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Biometrics; Cryptic species; Genotype; Orbulina universa; Planktonic foraminifera; Shell porosity

Indexed keywords

BIOMETRY; DNA; MORPHOLOGY; OLIGOTROPHIC ENVIRONMENT; PALEOCEANOGRAPHY; PLANKTONIC FORAMINIFERA; POROSITY; PRINCIPAL COMPONENT ANALYSIS; SHELL; SPECIES OCCURRENCE; SURFACE WATER;

ATLANTIC OCEAN; INDIAN OCEAN; PACIFIC OCEAN;

FORAMINIFERA; ORBULINA UNIVERSA;

EID: 67349189510     PISSN: 03778398     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.marmicro.2009.03.001     Document Type: Article

References (93)

1. Aitchison J. The statistical analysis of compositional data (2003), Blackburn, Caldwell
2. Anand P., Elderfield H., and Conte M.H. Calibration of Mg/Ca thermometry in planktonic foraminifera from a sediment trap time series. Paleoceanography 18 (2003) 28-31
3. Arnold A.J., and Parker W.C. Biogeography of planktonic Foraminifera. In: Gupta B.K.S. (Ed). Modern Foraminifera (1999), Kluwer Academic Publishers 103-122
4. Bandy O.L. Variations in Globigerina bulloides d'Orbigny as indices of water masses. Antarctic Journal of the U.S. 7 (1972) 194-195
5. Bauch D., Darling K.F., Simstich J., Bauch H.A., and Erlenkeuser H. Palaeoceanographic implications of genetic variation in living North Atlantic Neogloboquadrina pachyderma. Nature 424 (2003) 299-302
6. Bé A.W.H. Shell porosity of Recent planktonic foraminifera as a climatic index. Science 161 (1968) 881-884
7. Bé A.W.H. An ecological, zoogeographic and taxonomic review of Recent planktonic foraminifera. In: Ramsay A.T.S. (Ed). Oceanic Micropaleontology vol. 1 (1977), Academic Press, London 1-100
8. Bé A.W.H., and Duplessy J.-C. Subtropical convergence fluctuations and Quaternary climates in the middle latitudes of the Indian Ocean. Science 194 (1976) 419-422
9. Bé A.W.H., Harrison S.M., and Lott L. Orbulina universa d'Orbigny in the Indian Ocean. Micropaleontology 19 (1973) 150-192
10. Bé A.W.H., Hemleben C., Anderson O.R., and Spindler M. Pore structures in planktonic foraminifera. Journal for Foraminiferal Research 10 (1980) 117-128
11. Belkin I.M., and Gordon A.L. Southern Ocean fronts from the Greenwich meridian to Tasmania. Journal of Geophysical Research 101 (1996) 3675-3696
12. Bemis B.E., Spero H.J., Lea D.W., and Bijma J. Temperature influence on the carbon isotopic composition of Globigerina bulloides and Orbulina universa (planktonic foraminifera). Marine Micropaleontology 38 (2000) 213-228
13. Bijma J., Faber Jr. W.W., and Hemleben C. Temperature and salinity limits for growth and survival of some planktonic foraminifers in laboratory cultures. Journal of Foraminiferal Research 20 (1990) 95-116
14. Bijma J., Hemleben C., Huber B.T., Erlenkeuser H., and Kroon D. Experimental determination of the ontogenetic stable isotope variability in two morphotypes of Globigerinella siphonifera (d'Orbigny). Marine Micropaleontology 35 (1998) 141-160
15. Billups K., and Spero H.J. Relationship between shell size, thickness and stable isotopes in individual planktonic foraminifera from two equatorial Atlantic cores. Journal of Foraminiferal Research 25 (1995) 24-37
16. Brayard A., Escarguel G., and Bucher H. Latitudinal gradient of taxonomic richness: combined outcome of temperature and geographic mid-domains effects?. Journal of Zoological Systematics and Evolutionary Research 43 (2005) 178-188
17. Caron D.A., Anderson O.R., Lindsey J.L., Faber Jr. W.W., and Lim E.L. Effects of gametogenesis on the test structure and dissolution of some spinose planktonic foraminifera and implications for test preservation. Marine Micropaleontology 16 (1990) 93-116
18. Chayes F. On correlation between variables of constant sum. Journal of Geophysical Research 65 12 (1960) 4185-4193
19. CLIMAP Project Members. The surface of the ice-age Earth. Science 191 (1976) 1131-1144
20. Colombo M.R., and Cita M.B. Changes in size and test porosity of Orbulina universa d'Orbigny in the Pleistocene record of Cape Bojador (DSDP Site 397, Eastern North Atlantic). Marine Micropaleontology 5 (1980) 13-29
21. Darling K.F., and Wade C.M. The genetic diversity of planktonic foraminifera and the global distribution of ribosomal RNA genotypes. Marine Micropaleontology 67 (2008) 216-238
22. Darling K.F., Wade C.M., Kroon D., and Leigh Brown A.J. The diversity and distribution of modern planktic foraminiferal SSU rRNA genotypes and their potential as tracers of present and past ocean circulations. Paleoceanography 14 (1999) 3-12
23. Darling K.F., Wade C.M., Stewart I.A., Kroon D., Dingle R., and Leigh Brown A.J. Molecular evidence for genetic mixing of Arctic and Antarctic subpolar populations of planktonic foraminifers. Nature 405 (2000) 43-47
24. Darling K.F., Kucera M., Pudsey C.J., and Wade C.M. Molecular evidence links cryptic diversification in polar planktonic protists to Quaternary climate dynamics. Proceedings of the National Academy of Science 101 (2004) 7657-7662
25. Darling K.F., Kucera M., Kroon D., and Wade C.M. A resolution for the coiling direction paradox in Neogloboquadrina pachyderma. Paleoceanography 21 (2006) 1-14
26. Darling K.F., Kucera M., and Wade C. Global molecular phylogeography reveals persistent Arctic circumpolar isolation in a marine planktonic protist. Proceedings of the National Academy of Science 104 (2007) 5002-5007
27. de Garidel-Thoron, 2001. Dynamique climatique de l'Océan Pacifique ouest équatorial au cours du Pleistocène récent, Ph.D. dissertation, Université Aix-Marseille III.
28. Deuser W.G. Seasonal variations in isotopic composition and deep-water fluxes of the tests of perennially abundant planktonic foraminifera of the Sargasso Sea: results from sediment-trap collections and their paleoceanographic significance. Journal of Foraminiferal Research 17 (1987) 14-27
29. Deuser W.G., Ross E.H., Hemleben C., and Spindler M. Seasonal changes in species composition, numbers, mass size, and isotopic composition of planktonic foraminifera settling into the deep Sargasso Sea. Palaeogeography Palaeoclimatology Palaeocology 33 (1981) 103-127
30. de Vargas C., Zaninetti L., Hilbrecht H., and Pawlowski J. Phylogeny and rates of molecular evolution of planktonic foraminifera: SSU rDNA sequences compared to the fossil record. Journal of Molecular Evolution 45 (1997) 285-294
31. de Vargas C., Norris R.D., Zaninetti L., Gibb S.W., and Pawlowski J. Molecular evidence of cryptic speciation in planktonic foraminifers and their relation to oceanic provinces. Proceedings of the National Academy of Science 96 (1999) 2864-2868
32. de Vargas C., Renaud S., Hilbrecht H., and Pawlowski J. Pleistocene adaptive radiation in Globorotalia truncatulinoides: genetic, morphologic, and environmental evidence. Paleobiology 27 (2001) 104-125
33. de Vargas C., Bonzon M., Rees N.W., Pawlowski J., and Zaninetti L. A molecular approach to biodiversity and biogeography in the planktonic foraminifer Globigerinella siphonifera (d'Orbigny). Marine Micropaleontology 45 (2002) 101-116
34. de Vargas C., Saez A.G., Medlin L., and Thierstein H.R. Super-species in the calcareous plankton. In: Thierstein H.R., and Young J.R. (Eds). Coccolithophores, from Molecular Processes to Global Impact (2003), Springer, Berlin 271-298
35. Eggins S.E., Sadekov A., and de Deckker P. Modulation and daily banding of Mg/Ca in Orbulina universa tests by symbiont photosynthesis and respiration: a complication for seawater thermometry?. Earth and Planetary Science Letters 225 (2004) 411-419
36. Emiliani C. Depth habitats of some species of pelagic foraminifera as indicated by oxygen isotope ratios. American Journal of Science 252 (1954) 269-324
37. Ericson D.B. Coiling direction of Globigerina pachyderma as a climatic index. Science 130 (1959) 219-220
38. Escarguel G., Brayard A., and Bucher H. Evolutionary rates do not drive latitudinal diversity gradients. Journal of Zoological Systematics and Evolutionary Research 46 (2008) 82-86
39. Fischer, G., Wefer, G., 1999. Use of proxies in paleoceanography. Springer Verlag, Berlin.
40. Fisher C. Planktonic foraminiferal porosity: a water mass proxy for latest Cenomanian paleoceanography, Greenhorn Sea, Western Interior USA and Canada. Cretaceous Research 24 (2003) 633-651
41. Fisher C., Sageman B.B., Asure S.E., Acker B., and Mahar Z. Planktic foraminiferal porosity as a tool for paleoceanographic reconstruction, Mid-Cretaceous Western Interior Sea. Palaios 18 (2003) 34-46
42. Frerichs W.E., Heiman M.E., Borgman L., and Bé A.W.H. Latitudinal variations in planktonic foraminiferal test porosity: Part 1. Optical studies. Journal of Foraminiferal Research 2 (1972) 6-13
43. Haenel P. Intérêt paléoocéanographique d'Orbulina universa d'Orbigny (foraminifère). Oceanologica Acta 10 (1987) 15-25
44. Hallock P. Fluctuations in the trophic resource continuum: a factor in global diversity cycles?. Paleoceanography 2 (1987) 457-471
45. Hammer Ø., Harper D.A.T., and Ryan P.D. PAST: Paleontological Statistics Software Package for Education and Data Analysis. Palaeontologia Electronica 4 (2001) 9. http://palaeo-electronica.org/2001_1/past/issue1_01.htm (http://palaeo-electronica.org/2001_1/past/issue1_01.htm)
46. Healy-Williams N. Stables isotopes differences among morphotypes of Neogloboquadrina pachyderma (Ehrenberg): implications for high-latitude palaeoceanographic studies. Terra Nova 4 (1992) 693-700
47. Healy-Williams N., Ehrlich R., and Williams D.F. Morphometric and stable isotopic evidence for subpopulations of Globorotalia truncatulinoides. Journal of Foraminiferal Research 15 (1985) 242-253
48. Hemleben C., Spindler M., and Anderson O.R. Modern Planktonic Foraminifera (1989), Springer, New York
49. Hecht A.D. Intraspecific variation in recent populations of Globigerinoides ruber and Globigerinoides trilobus and their application to paleoenvironmental analysis. Journal of Paleontology 48 (1974) 1217-1234
50. Hecht A.D., and Savin S.L. Phenotypic variation and oxygen isotope ratios in recent planktonic foraminifera. Journal of Foraminiferal Research 2 (1972) 55-67
51. Hecht A.D., Bé A.W.H., and Lott L. Ecologic and paleoclimatic implications of morphologic variation of Orbulina universa in the Indian Ocean. Science 194 (1976) 422-424
52. Hooker S.B., Rees N.W., and Aiken J. An objective methodology for identifying oceanic provinces. Progress in Oceanography 45 (2000) 313-338
53. Huber B.T., Bijma J., and Darling K.F. Cryptic speciation in the living planktonic foraminifer Globigerinella siphonifera (d'Orbigny). Paleobiology 23 (1997) 33-62
54. Hutson W.H. Transfer functions under no-analog conditions: experiments with Indian Ocean planktonic foraminifera. Quaternary Research 8 (1977) 355-367
55. Imbrie J., and Kipp N.G. In: Turekian K.K. (Ed). A new micropaleontological method for quantitative paleoclimatology: application to a late Pleistocene Caribbean core (1971), The Late Cenozoic Glacial Ages Yale university press, New Haven
56. Kennett J.P. Globorotalia truncatulinoides as a paleo-oceanographic index. Science 159 (1968) 1461-1463
57. Kennett J.P. Latitudinal variation in Globigerina pachyderma (Ehrenberg) in surface sediments of the southwest Pacific Ocean. Micropaleontology 14 (1968) 305-318
58. Kennett J.P. Phenotypic variation in some Recent and late Cenozoic planktonic foraminifera. In: Hedley R.H., and Adams C.G. (Eds). Foraminifera vol. 2 (1976), Academy Press, New York 111-170
59. Kennett J.P. Marine Geology (1982), Prentice-Hall, Englewood Cliffs, NJ
60. Knowlton N. Sibling species in the sea. Annual Review of Ecology and Systematics, 24 (1993) 189-216
61. Kölher-Rink S., and Khül M. The chemical microenvironment of the symbiotic planktonic foraminifer Orbulina universa. Marine Biology Research 1 (2005) 68-78
62. Kucera M., and Darling K.F. Cryptic species of planktonic foraminifera: their effect on palaeoceanographic reconstructions. Philosophical Transaction of The Royal Society of London 360 (2002) 695-718
63. Kucera M., Rosell-Melé A., Schneider R., Waelbroeck C., and Weinelt M. Multiproxy approach for the reconstruction of the glacial ocean surface (MARGO). Quaternary Science Reviews 24 (2005) 813-819
64. Kucera M., et al. Reconstitution of sea-surface temperatures from assemblages of planktonic foraminifera: multi technique approach based on geographically constrained calibration data sets and its application to glacial Atlantic and Pacific Oceans. Quaternary Science Reviews 24 (2005) 951-998
65. Lea D.W., Martin P.A., Chan D.A., and Spero H.J. Calcium uptake and calcification rate in the planktonic foraminifera Orbulina universa. Journal of Foraminiferal Research 25 (1995) 14-23
66. Lipps J.H. Plankton evolution. Evolution 24 (1970) 1-22
67. Lipps J.H. Fossil Prokaryotes and Protists (1992), Blackwell Science, Cambridge, MA
68. Lourens L.J., Hilgen F.J., Laskar J., Shackleton N.J., and Wilson D.S. The Neogene Period. In: Gradstein F.M., Ogg J.G., and Smith A.G. (Eds). A geologic Time Scale 2004 (2005), Cambridge University Press, Cambridge, UK 409-440
69. Malmgren B.A., and Kennett J.P. Biometric analysis of phenotypic variation: Globigerina pachyderma (Ehrenberg) in the South Pacific Ocean. Micropaleontology 18 (1972) 241-248
70. Malmgren B.A., and Kennett J.P. Biometric analysis of phenotypic variation in recent Globigerina bulloides (d'Orbigny) in the southern Indian Ocean. Marine Micropaleontology 1 (1976) 3-25
71. Malmgren B., and Kennett J.P. Late quaternary paleoclimatic applications of mean size variations in Globigerina bulloides d'Orbigny in the southern Indian Ocean. Journal of Paleontology 52 (1978) 1195-1207
72. Malmgren B., and Healy-Williams N. Variation in test diameter of Orbulina universa in the paleoclimatology of the late quaternary of the Gulf of Mexico. Palaeogeography, Palaeoclimatology, Palaeocology 25 (1978) 235-240
73. Malmgren B.A., Kucera M., Nyberg J., and Waelbroeck C. Comparison of statistical and artificial neural network techniques for estimating pastsea-surface temperatures from planktonic foraminifer census data. Paleoceanography 16 (2001) 520-530
74. Metzl N. Le programme OISO, Service d'Observation de l'Océan Indien. Lettre IGBP/France 10 (2000) 79-83
75. Mix A.C., Bard E., and Schneider R. Environmental processes of the ice age: land, oceans, glaciers (EPILOG). Quaternary Science Reviews 20 (2001) 627-657
76. Morey A.E., Mix A.C., and Pisias N.G. Planktonic foraminiferal assemblages preserved in surface sediments correspond to multiple environmental variables. Quaternary Science Reviews 24 (2005) 925-950
77. Orr W.N. Variation and distribution of Globigerinoides ruber in the Gulf of Mexico. Micropaleontology 15 (1969) 373-379
78. Parker F.L. Planktonic foraminiferal species in Pacific sediments. Micropaleontology 8 (1962) 219-254
79. Robins D.B., and Aiken J. The Atlantic Meridional Transect: an oceanographic research program to investigate physical, chemical, biological and optical variables of the Atlantic Ocean. Underwater Technol. 21 (1996) 8-14
80. Robbins L.L., and Healy-Williams N. Toward a classification of planktonic foraminifera based on biochemical, geochemical, and morphological criteria. Journal of Foraminiferal Research 21 2 (1991) 159-167
81. Rutherford S., D'Hondt S., and Prell W. Environmental controls on the geographic distribution of zooplankton diversity. Nature 400 (1999) 749-753
82. Sokal R.R., and Rohlf F.J. Biometry: The Principles and Practice of Statistics in Biological Research (1995), Freeman, New York 887 pp.
83. Sandford R.F., Pierson C.T., and Crovelli R.A. An objective replacement method for censored geochemical data. Mathematical Geology 25 (1993) 59-80
84. Spero H.J. Symbiosis in the planktonic foraminifer Orbulina universa and the isolation of its symbiotic dinoflagellate Gymnodinium béii sp. Nov. Journal of Phycology 23 (1987) 307-317
85. 13C data. Nature 335 (1988) 717-719
86. Spero H.J., Bijma J., Lea D.W., and Bemis B.E. Effect of seawater carbonate concentration on foraminiferal carbon and oxygen isotopes. Nature 390 (1997) 497-499
87. Stewart I.A., Darling K.F., Kroon D., Wade C.M., and Troelstra S.R. Genotypic variability in subarctic Atlantic planktic foraminifera. Marine Micropaleontology 43 (2001) 143-153
88. Tomczak M., and Godfrey J.S. Regional Oceanography: an Introduction 2nd edn (2003) (2003), Daya Publishing House, Delhi 390 pp.
89. Wade B.D., and Garcia-Pichel F. Evaluation of DNA extraction methods for molecular analyses of microbial communities in modern calcareous microbialites. Geomicrobiology Journal 20 (2003) 549-561
90. Wiebe P.H., Morton A.W., Bradley A.M., Backus R.H., Craddock J.E., Barber V., Cowles T.J., and Flierl G.R. New developments in the MOCNESS, an apparatus for sampling zooplankton and micronekton. Marine Biology 87 (1985) 313-323
91. Williams D.F., Ehrlich R., Spero H.J., Healy-Williams N., and Gary A.C. Shape and isotopic differences between conspecific foraminiferal morphotypes and resolution of paleoceanographic events. Palaeogeography Palaeoclimatology Palaeoecology 64 (1988) 153-162
92. Wolf-Gladrow D.A., Bijma J., and Zeebe R.E. Model simulation of the carbonate chemistry in the microenvironment of symbiont bearing foraminifera. Marine Chemistry 64 (1999) 181-198
93. Zeebe R.E., Bijma J., and Wolf-Gladrow D.A. A diffusion-reaction model of carbon isotope fractionation in foraminifera. Marine Chemistry 64 (1999) 199-227