Functional diversity in cryptic species of Chaetoceros socialis Lauder (Bacillariophyceae)

Journal of Plankton Research

Volumn 34, Issue 5, 2012, Pages 416-431

  Degerlund, Maria ^a   Huseby, Siv ^a   Zingone, Adriana ^b   Sarno, Diana ^b   Landfald, Bjarne ^a  

^a UNIVERSITY OF TROMSØ   (Norway)

^b STAZIONE ZOOLOGICA ANTON DOHRN   (Italy)

Author keywords

cosmopolitan; cryptic diversity; diatoms; functional diversity; species concept

Indexed keywords

ALLOPATRY; DIATOM; FUNCTIONAL ROLE; GEOGRAPHICAL DISTRIBUTION; LOW TEMPERATURE; MARINE ECOSYSTEM; MOLECULAR ANALYSIS; PHENOTYPIC PLASTICITY; PHOTOSYNTHESIS; PHYLOGENETICS; PHYTOPLANKTON; SPECIES CONCEPT; TAXONOMY;

ARCTIC OCEAN; ATLANTIC OCEAN; ATLANTIC OCEAN (NORTHEAST); MEDITERRANEAN SEA; TYRRHENIAN SEA;

BACILLARIOPHYCEAE; BACILLARIOPHYTA; BACTERIA (MICROORGANISMS); CHAETOCEROS SOCIALIS;

EID: 84859392342     PISSN: 01427873     EISSN: 14643774     Source Type: Journal    
DOI: 10.1093/plankt/fbs004     Document Type: Article

References (100)

1. Alverson, A. J. (2008) Molecular systematics and the diatom species. Protist, 159, 339-353.
2. Amato, A., Kooistra, W. H. C. F., Levialdi Ghiron, J. H. et al. (2007) Reproductive isolation among sympatric cryptic species in marine diatoms. Protist, 158, 193-207.
3. Amato, A., Orsini, L., D'Alelio, D. et al. (2005) Life cycle, size reduction patterns, and ultrastructure of the pennate planktonic diatom Pseudonitzschia delicatissima (Bacillariophyceae). J. Phycol., 41, 542-556.
4. Armbrust, E. V. and Chisholm, S. W. (1992) Patterns of cell size change in a marine centric diatom: variability evolving from clonal isolates. J. Phycol., 28, 146-156.
5. Assmy, P., Hernández-Becerril, D. U. and Montresor, M. (2008) Morphological variability and life cycle traits of the type species of the diatom genus Chaetoceros, C. dichaeta. J. Phycol., 44, 152-163.
6. Baker, J. W., James, P., Grover, J. P. et al. (2009) Growth at the edge of the niche: an experimental study of the harmful alga Prymnesium parvum. Limnol. Oceanogr., 54, 1679-1687.
7. Balzano, S., Sarno, D. and Kooistra, W. H. C. F. (2011) Effects of salinity on the growth rate and morphology of ten Skeletonema strains. J. Plankton Res., 33, 937-945.
8. Bode, A. and Varela, M. (1998) Primary production and phytoplankton in three Galician Rias Altas (NW Spain): seasonal and spatial variability. Sci. Mar., 62, 319-330.
9. Booth, B. C., Larouche, P., Bélanger, S. et al. (2002) Dynamics of Chaetoceros socialis blooms in the North Water. Deep-Sea Res. Part II, 49, 5003-5025.
10. Brand, L. E. (1981) Genetic variability in reproduction rates in marine phytoplankton populations. Evolution, 35, 1117-1127.
11. Cerino, F., Orsini, L., Sarno, D. et al. (2005) The alternation of different morphotypes in the seasonal cycle of the toxic diatom Pseudo-nitzschia galaxiae. Harmful Algae, 4, 33-48.
12. Chepurnov, V. A., Mann, D. G., Sabbe, K. et al. (2004) Experimental studies on sexual reproduction in diatoms. Internat. Rev. Cytol., 237, 91-154.
13. Cleve, P. T. (1896) Diatoms from Baffins Bay and Davis Strait. Bihang till K. Svenska Vet.-Akad. Handlingar, 22, 1-22.
14. Coleman, A. (2009) Is there a molecular key to the level of 'biological species' in eukaryoteš A DNA guide. Mol. Phylogenet. Evol., 50, 197-203.
15. Costello, J. C. and Chisholm, S. W. (1981) The influence of cell size on the growth rate of Thalassiosira weissflogii. J. Plankton Res., 3, 415-419.
16. D'Alelio, D., Amato, A., Luedeking, A. et al. (2009) Sexual and vegetative phases in the planktonic diatom Pseudo-nitzschia multistriata. Harmful Algae, 8, 225-232.
17. D'Alelio, D., Ribera d'Alcalà, M., Dubroca, L. et al. (2010) The time for sex: a biennial life cycle in a marine planktonic diatom. Limnol. Oceanogr., 55, 106-114.
18. Dayrat, B. (2005) Towards integrative taxonomy. Biol. J. Linn. Soc., 85, 407-415.
19. Degerlund, M. and Eilertsen, H. C. (2010) Main species characteristics of phytoplankton spring blooms in NE Atlantic and Arctic waters (68-808N). Est. Coasts, 33, 242-269.
20. de Queiroz, K. (2007) Species concepts and species delimitation. Syst. Biol., 56, 879-886.
21. Dimier, C., Corato, F., Tramontano, F. et al. (2007) Photoprotection and xanthophyll-cycle activity in three marine diatoms. J. Phycol., 43, 937-947.
22. Eilertsen, H. C., Schei, B. and Taasen, J. P. (1981) Investigations on the plankton community of Balsfjorden, northern Norway. The phytoplankton 1976-1978. Abundance, species composition, and succession. Sarsia, 66, 129-141.
23. Eilertsen, H. C. and Skarohamar, J. (2006) Temperatures of north Norwegian fjords and coastal waters: variability, significance of local processes and air-sea heat exchange. Est. Coast. Shelf Sci., 67, 530-538.
24. Ellegaard, M., Godhe, A., Härnström, K. et al. (2008) The species concept in a marine diatom: LSU rDNA-based phylogenetic differentiation in Skeletonema marinoi/dohrnii (Bacillariophyceae) is not reflected in morphology. Phycologia, 47, 156-167.
25. Evans, K. M., Chepurnov, V. A., Sluiman, H. J. et al. (2009) Highly differentiated populations of the freshwater diatom Sellaphora capitata suggest limited dispersal and opportunities for allopatric speciation. Protist, 160, 386-396.
26. Evensen, D. L. and Hasle, G. R. (1975) The morphology of some Chaetoceros (Bacillariophyceae) species as seen in the electron microscope. Nova Hedwigia Beih., 53, 153-174.
27. Fenchel, T. (2005) Cosmopolitan microbes and their cryptic species. Aquat. Microb. Ecol., 41, 49-54.
28. Finlay, B. J. (2002) Global dispersal of free-living microbial eukaryote species. Science, 296, 1061-1063.
29. Finlay, B. J., Esteban, G. F. and Fenchel, T. (2004) Protist diversity is different? Protist, 155, 15-22.
30. Fraser, C., Alm, E. J., Polz, M. F. et al. (2009) The bacterial species challenge: making sense of genetic and ecological diversity. Science, 323, 741-746.
31. Gilstad, M. and Sakshaug, E. (1990) Growth rates of ten diatoms species from the Barents Sea at different irradiances and day lengths. Mar. Ecol. Prog. Ser., 64, 169-173.
32. Gran, H. H. (1897) Botany. Protophyta: Diatomaceae, Silicoflagellata and Cilioflagellata. The Norwegian North-Atlantic Expedition 1876-1878.
33. Grøndahl & Søn Christiania 36. Guillard, R. R. L. and Ryther, J.H. 1962) Studies of marine plankton diatoms. I. Cyclotella nana Hustedt and Detonula confervacea (Cleve) Gran. Can. J. Microbiol., 8, 229-239.
34. Guiry, M. D. (2011) Chaetoceros compressus. In: Guiry, M. D. and Guiry, G. M. (eds), (2011). AlgaeBase. World-wide Electronic Publication, National University of Ireland, Galway. Accessed through: World Register of Marine Species at http://www.marinespecies .org/aphia.php?p=taxdetails&id=149129 (16 December 2011).
35. Hargraves, P. E. (1979) Studies on marine plankton diatoms IV. Morphology of Chaetoceros resting spores. Nova Hedwigia Beih., 64, 99-120.
36. Hasle, G. R. (1976) The biogeography of some marine planktonic diatoms. Deep-Sea Res., 23, 319-338.
37. Hasle, G. R. (2002) Are most domoic acid-producing species of the diatom genus Pseudo-nitzschia cosmopoliteš Harmful Algae, 1, 137-146.
38. Hasle, G. R. and Syvertsen, E. E. (1997) Marine diatoms. In Tomas, C. R. (ed.) Identifying Marine Phytoplankton. Academic Press, San Diego, pp. 5-385.
39. Higgins, D., Thompson, J., Gibson, T. et al. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res., 22, 4673-4680.
40. Holm-Hansen, O. and Riemann, B. (1978) Chlorophyll a determination: improvements in methodology. Oikos, 30, 438-447.
41. Ishii, K.-I., Iwataki, M., Matsuoka, K. et al. (2011) Proposal of identification criteria for resting spores of Chaetoceros species (Bacillariophyceae) from a temperate coastal sea. Phycologia, 50, 351-362.
42. Jensen, K. G. and Moestrup, ø. (1998) The genus Chaetoceros (Bacillariophyceae) in inner Danish coastal waters. Opera Bot., 133, 1-68.
43. Jewson, D. H. (1992) Size reduction, reproductive strategy and the life cycle of a centric diatom. Philos. Trans. R. Soc. Lond. B, 336, 191-213.
44. Kagami, M. and Urabe, J. (2001) Phytoplankton growth rate as a function of cell size: an experimental test in Lake Biwa. Limnology, 2, 111-117.
45. Koester, J. A., Swalwell, J. E., von Dassow, P. et al. (2010) Genome size differentiates co-occurring populations of the planktonic diatom Ditylum brightwellii (Bacillariophyta). BMC Evol. Biol., 10, 1. Doi:10.1186/1471-2148- 10-1.
46. Kooistra, W. H. C. F., Gersonde, R., Medlin, L. K. et al. (2007) The origin and evolution of the diatoms: their adaptation to a planktonic existence. In Falkowski, P. G. and Knoll, A. H. (eds), Evolution of Primary Producers in the Sea. Elsevier Academic Press, Burlington, pp. 207-249.
47. Kooistra, W. H. C. F., Sarno, D., Balzano, S. et al. (2008) Global diversity and biogeography of Skeletonema species (Bacillariophyta). Protist, 159, 177-193.
48. Kooistra, W. H. C. F., Sarno, D., Hernández-Becerril, D. U. et al. (2010) Comparative molecular and morphological phylogenetic analyses of taxa in the Chaetocerotaceae (Bacillariophyta). Phycologia, 49, 471-500.
49. Kudo, I. (2003) Change in the uptake and cellular Si:N ratio in diatoms responding to the ambient Si:N ratio and growth phase. Mar. Biol., 143, 39-46
50. Lauder, H. S. (1864) Remarks on the marine diatomaceae found at Hong Kong, with descriptions of new species. Trans. R. Microsc. Soc. Lond., New Series, 12, 75-79.
51. Leaners, G., Maroteaux, L., Michot, B. et al. (1989) Dinoflagellates in evolution. A molecular phylogenetic analysis of large subunit ribosomal RNA. J. Mol. Evol., 29, 40-51.
52. Leu, E., Falk-Petersen, S. and Hessen, D. O. (2007) Ultraviolet radiation affects growth but not food quality of arctic diatoms. Limnol. Oceanogr., 52, 787-797.
53. Lowe, C. D., Day, A., Kemp, S. J. et al. (2005) There are high levels of functional and genetic diversity in Oxyrrhis marina. J. Eukaryot. Microbiol., 52, 250-257.
54. Lowe, C. D., Keeling, P. J., Martin, L. E. et al. (2011) Who is Oxyrrhis marina? Morphological and phylogenetic studies on an unusual dinoflagellate. J. Plankton Res., 33, 555-567.
55. Mann, D. G. (1988) Why didn't Lund see sex in Asterionella? A discussion of the diatom life cycle in nature. In Round, F. E. (ed.), Algae and the Aquatic Environment. Biopress, Bristol, pp. 384-412.
56. Mann, D. G. (1999) The species concept in diatoms. Phycologia, 38, 437-495.
57. Maumus, F., Allen, A. E., Mhiri, C. et al. (2009) Potential impact of stress activated retrotransposons on genome evolution in a marine diatom. BMC Genomics, 10, 624. doi:10.1186/ 1471-2164-10-624.
58. McBride, B. B., Muller-Parker, G. and Jakobsen, H. H. (2009) Low thermal limit of growth rate of Symbiodinium californium (Dinophyta) in culture may restrict the symbiont to southern populations of its host anemones (Anthopleura spp.; Anthozoa, Cnidaria). J. Phycol., 45, 855-863.
59. McDonald, S. M., Sarno, D. and Zingone, A. (2007) Identifying Pseudo-nitzschia species in natural samples using genus-specific primers and clone libraries. Harmful Algae, 6, 849-860.
60. McManus, G. B. and Katz, L. A. (2009) Molecular and morphological methods for identifying plankton: what makes a successful marriage? J. Plankton Res., 31, 1119-1129.
61. Menden-Deuer, S. and Lessard, E. J. (2000) Carbon to volume relationships for dinoflagellates, diatoms and other protist plankton. Limnol. Oceanogr., 45, 569-579.
62. Moniz, M. B. J. and Kaczmarska, I. (2010) Barcoding of diatoms: nuclear encoded ITS revisited. Protist, 161, 7-34
63. Montresor, M., Sgrossi, S., Procaccini, G. et al. (2003) Intraspecific diversity in Scrippsiella trochoidea (Dinophyceae): evidence for cryptic species. Phycologia, 42, 56-70.
64. Olenina, I., Hajdu, S., Eder, L. et al. (2006) Biovolumes and sizeclasses of phytoplankton in the Baltic Sea. HELCOM Balt. Sea Environ. Proc., 106, 1-144
65. Orsini, L., Procaccini, G., Sarno, D. et al. (2004) Multiple rDNA ITS-types within the diatom Pseudo-nitzschia delicatissima (Bacillariophyceae) and their relative abundances across a spring bloom in the Gulf of Naples. Mar. Ecol. Prog. Ser., 271, 87-98.
66. Poulíčková, A., Špačková, J., Kelly, M. G. et al. (2008) Ecological variation within Sellaphora species complexes (Bacillariophyceae): specialists or generalistš Hydrobiologia, 614, 373-386.
67. Poulíčková, A., Veselá, J., Neustupa, J. et al. (2010) Pseudocryptic diversity versus cosmopolitanism in diatoms: a case study on Navicula cryptocephala Kütz. (Bacillariophyceae) and morphologically similar taxa. Protist, 161, 353-369.
68. Proschkina-Lavrenko, A. I. (1953) Species Chaetoceros novae et curiosae Maris Nigri I. Botanicheskie materialy, Otdela sporovykhastenii. Akad. NAUK SSSR, 9, 46-56.
69. Proschkina-Lavrenko, A. I. (1963) Diatomovye vodorosli planktona Azovskogo Morja. Akad. NAUK SSSR, Moskva, pp. 190.
70. Ribera D'Alcalà, M., Conversano, F., Corato, F. et al. (2004) Seasonal patterns in plankton communities in a pluriannual time series at a coastal Mediterranean site (Gulf of Naples): an attempt to discern recurrences and trends. Sci. Mar., 68, 65-83.
71. Rines, J. E. B., Donaghay, P. L., Dekshenieks, M. M. et al. (2002) Thin layers and camouflage: hidden Pseudo-nitzschia spp. (Bacillariophyceae) populations in a fjord in the San Juan Islands, Washington, USA. Mar. Ecol. Prog. Ser., 225, 123-137.
72. Rodríguez, F., Derelle, E., Guillou, L. et al. (2005) Ecotype diversity in the marine picoeukaryote Ostreococcus (Chlorophyta, Prasinophyceae). Environ. Microbiol., 7, 853-859.
73. Ronquist, F. and Huelsenbeck, J. P. (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572-1574.
74. Rosselló-Mora, R., Lucio, M., Peña, A. et al. (2008) Metabolic evidence for biogeographic isolation of the extremophilic bacterium Salinibacter ruber. ISME J., 2, 242-253.
75. Rynearson, T. A. and Armbrust, E. V. (2004) Genetic differentiation among populations of the planktonic marine diatom Ditylum brightwellii (Bacillariophyceae). J. Phycol., 40, 34-43.
76. Sàez, A. G., Probert, I., Geisen, M. et al. (2003) Pseudo-cryptic speciation in coccolithophores. Proc. Natl Acad. Sci. USA, 100, 7163-7168.
77. Sar, E. A., Sunesen, I., Lavigne, A. S. et al. (2011) Thalassiosira rotula, a heterotypic synonym of Thalassiosira gravida: morphological evidence. Diatom Res., 26, 109-119.
78. Saravanan, V. and Godhe, A. (2010) Genetic heterogeneity and physiological variation among seasonally separated clones of Skeletonema marinoi (Bacillariophyceae) in the Gullmar Fjord, Sweden. Eur. J. Phycol., 45, 177-190.
79. Sarno, D., Kooistra, W. H. C. F., Balzano, S. et al. (2007) Diversity in the genus Skeletonema (Bacillariophyceae): III. Phylogenetic position and morphological variability of Skeletonema costatum and Skeletonema grevillei, with the description of Skeletonema ardens sp. nov. J. Phycol., 43, 156-170.
80. Sarno, D., Kooistra, W. H. C. F., Medlin, L. K. et al. (2005) Diversity in the genus Skeletonema (Bacillariophyceae): II. An assessment of the taxonomy of S. costatum-like species with the description of four new species. J. Phycol., 41, 151-176.
81. Sarthou, G., Timmermans, K. R., Blain, S. et al. (2005) Growth physiology and fate of diatoms in the ocean: a review. J. Sea Res., 53, 25-42.
82. Schlick-Steiner, B. C., Steiner, F. M., Seifert, B. et al. (2010) Integrative taxonomy: a multisource approach to exploring biodiversity. Annu. Rev. Entomol., 55, 421-438.
83. Scholin, C. A., Villac, M. C., Buck, K. R. et al. (1994) Ribosomal DNA sequences discriminate among toxic and non-toxic Pseudonitzschia species. Nat. Toxins, 2, 152-165.
84. Schütt F. 1895 Arten von chaetoceros und peragallia ein beitrag zur hochseeflora Berichte Der Deutschen Botanischen Gesellschaft 13 35-48.
85. Sharma, N. K. and Rai, A. K. (2011) Biodiversity and biogeography of microalgae: progress and pitfalls. Environ. Rev., 19, 1-15. doi:10.1139/A10-020.
86. Shevchenko, O. G., Orlova, T. Y. and Aizdaicher, N. A. (2008) Development of the diatom Chaetoceros socialis f. radians (Schütt) Proschkina-Lavrenko 1963 in laboratory culture. Russ. J. Mar. Biol., 34, 224-229.
87. Simonelli, P., Troedsson, C., Nejstgaard, J. C. et al. (2009) Evaluation of DNA extraction and handling procedures for PCR-based copepod feeding studies. J. Plankton Res., 31, 1465-1474.
88. Smayda, T. J. (1958) Biogeographical studies of marine phytoplankton. Oikos, 9, 158-191.
89. Syvertsen, E. E. (1977) Thalassiosira rotula and T. gravida: ecology and morphology. Nova Hedwigia Beih., 54, 99-112.
90. Tamura, K., Peterson, D., Peterson, N. et al. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol., 28, 2731-2739.
91. Thingstad, T. F., Bellerby, R. G. J., Bratbak, G. et al. (2008) Counterintuitive carbon-to-nutrient coupling in an Arctic pelagic ecosystem. Nature, 455, 387-391.
92. Tomaru, Y., Takao, Y., Suzuki, H. et al. (2009) Isolation and characterization of a single-stranded RNA virus infecting the bloom-forming diatom Chaetoceros socialis. Appl. Environ. Microbiol, 75, 2375-2381.
93. Valdecasas, A. G., Williams, D. and Wheeler, Q. D. (2008) Integrative taxonomy then and now: a response to Dayrat (2005). Biol. J. Linn. Soc., 93, 211-216.
94. Vidoudez, C. and Pohnert, G. (2011) Comparative metabolomics of the diatom Skeletonema marinoi in different growth phases. Metabolomics, doi:10.1007/s11306-011-0356-6.
95. von Dassow, P., Chepurnov, V. A. and Armbrust, V. G. (2006) Relationships between growth rate, cell size, and induction of spermatogenesis in the centric diatom Thalassiosira weissflogii (Bacillariophyta). J. Phycol., 42, 887-899.
96. Will, K. W., Mishler, B. D. and Wheeler, Q. D. (2005) The perils of DNA barcoding and the need for integrative taxonomy. Syst. Biol., 54, 844-851.
97. Wood, M. A. and Leatham, T. (1992) The species concept in phytoplankton ecology. J. Phycol., 28, 723-729.
98. Yeates, D. K., Seago, A., Nelson, L. et al. (2010) Integrative or iterative taxonomy? Syst. Entomol. doi:10.1111/j.1365-3113.2010.00558.x.
99. Zak, J. C., Willig, M. R., Moorhead, D. L. et al. (1994) Functional diversity of microbial communities: a quantitative approach. Soil Biol. Biochem., 26, 1101-1108.
100. Zingone, A., Dubroca, L., Iudicone, D. et al. (2010) Coastal phytoplankton do not rest in winter. Est. Coasts, 33, 342-361.