Diatom cultures exhibit differential effects on larval metamorphosis in the marine gastropod Ilyanassa obsoleta (Say)

Journal of Experimental Marine Biology and Ecology

Volumn 379, Issue 1-2, 2009, Pages 51-59

  Leise, Esther M ^a   Froggett, Stephan J ^a   Nearhoof, Janice E ^b   Cahoon, Lawrence B ^b  

^a UNIVERSITY OF NORTH CAROLINA AT GREENSBORO   (United States)

^b UNIVERSITY OF NORTH CAROLINA WILMINGTON   (United States)

Author keywords

Caenogastropod; Coscinodiscus; Mollusc; Prosobranch; Snail; Tychopelagic

Indexed keywords

DIATOM; DIET; ENVIRONMENTAL CUE; GASTROPOD; JUVENILE; LARVAL DEVELOPMENT; METAMORPHOSIS; MUDFLAT; RECRUITMENT (POPULATION DYNAMICS); TESTING METHOD;

ATLANTIC COAST [NORTH AMERICA]; ATLANTIC COAST [UNITED STATES]; FRIDAY HARBOR; NORTH AMERICA; SAN JUAN ISLAND; SAN JUAN ISLANDS; UNITED STATES; WASHINGTON [UNITED STATES];

BACILLARIOPHYTA; CAENOGASTROPODA; COSCINODISCOPHYCEAE; COSCINODISCUS; COSCINODISCUS SP.; GASTROPODA; ILYANASSA; ILYANASSA OBSOLETA; MOLLUSCA;

EID: 70349217899     PISSN: 00220981     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jembe.2009.08.007     Document Type: Article

References (99)

1. Amspoker M.C., and McIntire C.D. Distribution of intertidal diatoms associated with the sediments in Yaquina estuary, Oregon. Journal of Phycology 14 (1978) 387-395
2. Atema J., and Burd G.D. A field study of chemotactic responses of the marine mud snail, Nassarius obsoletus. Journal of Chemical Ecology 1 (1975) 243-251
3. Bland M. An Introduction to Medical Statistics (1995), Oxford University Press, Oxford 396 pp.
4. Boettcher A.A., and Targett N.M. Induction of metamorphosis in queen conch, Strombus gigas Linnaeus, larvae by cues associated with red algae from their nursery grounds. Journal of Experimental Marine Biology and Ecology 196 (1996) 29-52
5. Bold H.C., and Wynne M.J. Introduction to the Algae: Structure and Reproduction (1985), Prentice-Hall, Inc., Englewood Cliffs, NJ 720 pp.
6. Brenchley G.A. Herbivory in juvenile Ilyanassa obsoleta (Neogastropoda). Veliger 30 (1987) 167-172
7. Bryan P.J., and Qian P.-Y. Induction of larval attachment and metamorphosis in the abalone Haliotis diversicolor (Reeve). Journal of Experimental Marine Biology and Ecology 223 (1998) 39-51
8. Cahoon L.B., and Laws R.A. Benthic diatoms from the North-Carolina continental-shelf-inner and mid shelf. Journal of Phycology 29 (1993) 257-263
9. Cahoon L.B., Nearhoof J.E., and Tilton C.L. Sediment grain size effect on benthic microalgal biomass in shallow aquatic ecosystems. Estuaries 22 (1999) 735-741
10. Cai Y., Deng C., and Liu Z. Studies on the ecology of Crassostrea rivularis (Gould) in Zhanjiang Bay. Tropical Oceanology/Redai Haiyang 11 (1992) 37-44
11. Cammen L.M., Blum U., Seneca E.D., and Stroud L.M. Energy flow in a North Carolina salt marsh: a synthesis of experimental and published data. ASB Bulletin 29 (1982) 111-134
12. Carr W.E.S. Chemoreception in the mud snail, Nassarius obsoletus. II. Identification of stimulatory substances. Biological Bulletin 133 (1967) 106-127
13. Carr W.E.S. Chemoreception in the mud snail, Nassarius obsoletus. I. Properties of stimulatory substances extracted from shrimp. Biological Bulletin 133 (1967) 90-105
14. Chiu J.M.Y., Thiyagarajan V., Pechenik J.A., Hung O.S., and Qian P.Y. Influence of bacteria and diatoms in biofilms on metamorphosis of the marine slipper limpet Crepidula onyx. Marine Biology 151 (2007) 1417-1431
15. Collier J. A bibliography of the marine mud snail Ilyanassa obsoleta. Invertebrate Reproduction and Development 42 (2002) 95-110
16. Connor M.S., and Edgar R.K. Selective grazing by the mud snail Ilyanassa obsoleta. Oecologia 53 (1982) 271-275
17. Connor M.S., Teal J.M., and Valiela I. The effect of feeding by mud snails, Ilyanassa obsoleta (Say), on the structure and metabolism of a laboratory benthic algal community. Journal of Experimental Marine Biology and Ecology 65 (1982) 29-45
18. Couper J.M., and Leise E.M. Serotonin injections induce metamorphosis in larvae of the gastropod mollusc Ilyanassa obsoleta. Biological Bulletin 191 (1996) 178-186
19. Cranford P.J. Behaviour and ecological importance of a mud snail (Ilyanassa obsoleta) population in a temperate macrotidal estuary. Canadian Journal of Zoology 66 (1988) 459-466
20. Curtis L.A. The influence of sex and trematode parasites on carrion response of the estuarine snail Ilyanassa obsoleta. Biological Bulletin 169 (1985) 377-390
21. Curtis L.A., and Hurd L.E. On the broad nutritional requirements of the mud snail, Ilyanassa (Nassarius) obsoleta (Say), and its polytrophic role in the food web. Journal of Experimental Marine Biology and Ecology 41 (1979) 289-297
22. Curtis L.A., and Hurd L.E. Nutrient procurement strategy of a deposit-feeding estuarine neogastropod, Ilyanassa obsoleta. Estuarine Coastal and Shelf Science 13 (1981) 277-285
23. Dobretsov S.V., Dahms H.-U., and Qian P.-Y. Inhibition of biofouling by marine microorganisms and their metabolites. Biofouling 22 (2006) 43-54
24. Dorsett D.A. Brains to cells: the neuroanatomy of selected gastropod species. In: Willows A.O.D. (Ed). The Mollusca: Neurobiology and Behavior, Part 2 (1986), Academic Press, Inc., Orlando 101-187
25. Doyle R.W. Settlement of planktonic larvae: a theory of habitat selection in varying environments. American Naturalist 109 (1975) 113-126
26. Froggett S.J., and Leise E.M. Metamorphosis in the marine snail Ilyanassa obsoleta, yes or NO?. Biological Bulletin 196 (1999) 57-62
27. Gallardo W.G., and Buen S.M.A. Evaluation of mucus, Navicula, and mixed diatoms as larval settlement inducers for the tropical abalone Haliotis asinina. Aquaculture 221 (2003) 357-364
28. Gentilcore L.R., and Derby C.D. Complex binding interactions between multicomponent mixtures and odorant receptors in the olfactory organ of the Caribbean spiny lobster Panulirus argus. Chemical Senses 23 (1998) 269-281
29. Gifondorwa D.J., and Leise E.M. Programmed cell death in the apical ganglion during larval metamorphosis of the marine mollusc Ilyanassa obsoleta. Biological Bulletin 210 (2006) 109-120
30. Gosner K.L. Guide to identification of marine and estuarine invertebrates. Cape Hatteras to the Bay of Fundy (1971), John Wiley and Sons, New York 693 pp.
31. Grossart H.P., and Simon M. Interactions of planktonic algae and bacteria: effects on algal growth and organic matter dynamics. Aquatic Microbial Ecology 47 (2007) 163-176
32. Grossart H.P., Levold F., Allgaier M., Simon M., and Brinkhoff T. Marine diatom species harbour distinct bacterial communities. Environmental Microbiology 7 (2005) 860-873
33. Hadfield M.G. The D.P. Wilson Lecture. Research on settlement and metamorphosis of marine invertebrate larvae: past, present and future. Biofouling 12 (1998) 9-29
34. Hadfield M.G. Why and how marine-invertebrate larvae metamorphose so fast. Cell and Developmental Biology 11 (2000) 437-443
35. Hadfield M.G., and Scheuer D. Evidence for a soluble metamorphic inducer in Phestilla: ecological, chemical and biological data. Bulletin of Marine Science 37 (1985) 556-566
36. 12C ratios. Ecology 60 (1979) 48-56
37. Hens M.D., Fowler K.A., and Leise E.M. Induction of metamorphosis decreases nitric oxide synthase gene expression in larvae of the marine mollusc Ilyanassa obsoleta (Say). Biological Bulletin 211 (2006) 208-211
38. 13C analysis. Journal of Experimental Marine Biology and Ecology 67 (1983) 227-242
39. Hunt J.H., Ambrose J.W.G., and Peterson C.H. Effects of the gastropod, Ilyanassa obsoleta (Say) and the bivalve, Mercenaria mercenaria (L.), on larval settlement and juvenile recruitment of infauna. Journal of Experimental Marine Biology and Ecology 108 (1987) 229-240
40. Hurd L.E. On the importance of carrion to reproduction in an omnivorous estuarine neogastropod, Ilyanassa obsoleta (Say). Oecologia 65 (1985) 513-515
41. Hustedt F. Marine Littoral Diatoms of Beaufort, North Carolina. Bulletin of the Duke University Marine Laboratory vol. 6 (1955) 67 pp.
42. Ingole B., Sivadas S., Goltekar R., Clemente S., Nanajkar M., Sawant R., D'Silva C., Sarkar A., and Ansari Z. Ecotoxicological effect of grounded MV River Princess on the intertidal benthic organisms off Goa. Environment International 32 (2006) 284-291
43. Ito S., and Kitamura H. Induction of larval metamorphosis in the sea cucumber Stichopus japonicus by periphitic diatoms. Hydrobiologia 358 (1997) 281-284
44. Jackson G.A. Interaction of physical and biological processes in the settlement of planktonic larvae. Bulletin of Marine Science 39 (1986) 202-212
45. Kasigwa P.F., and Mahika C.G. The diet of the edible cockle Anadara antiquata L. (Bivalvia, Arcidae) in Dar es Salaam, Tanzania, during the northeast monsoons. Hydrobiologia 209 (1991) 7-12
46. Kawamura T. The role of benthic diatoms in the early life stages of the Japanese abalone (Haliotis discus hannai). Survival Strategies in Early Life Stages of Marine Resources (1996), A.A. Balkema, Rotterdam 355-367
47. Kawamura T., Roberts R.D., and Takami H. A review of the feeding and growth of postlarval abalone. Journal of Shellfish Research 17 (1998) 615-625
48. Kawamura T., Saido T., Takami H., and Yamashita Y. Dietary value of benthic diatoms for the growth of post-larval abalone Haliotis discus hannai. Journal of Experimental Marine Biology and Ecology 194 (1995) 189-199
49. Kelaher B.P., Levinton J.S., and Hoch J.M. Foraging by the mud snail, Ilyanassa obsoleta (Say), modulates spatial variation in benthic community structure. Journal of Experimental Marine Biology and Ecology 292 (2003) 139-157
50. Kohn A.J. Feeding biology of gastropods. In: Saleuddin A.S.M., and Wilbur K.M. (Eds). The Mollusca: Physiology, Part 2 (1983), Academic Press, Inc., Orlando 1-63
51. Kozloff E.N. Seashore Life of the Northern Pacific Coast (1983), University of Washington Press, Seattle 370 pp.
52. Krug P.J., and Manzi A.E. Waterborne and surface-associated carbohydrates as settlement cues for larvae of the specialist marine herbivore Alderia modesta. Biological Bulletin 197 (1999) 97-103
53. Lam C., Harder T., and Qian P.-Y. Induction of larval settlement in the polychaete Hydroides elegans by extracellular polymers of benthic diatoms. Marine Ecology Progress Series 286 (2005) 145-154
54. Lau S.C.K., Thiyagarajan V., Cheung S.C.K., and Qian P.-Y. Roles of bacterial community composition in biofilms as a mediator for larval settlement of three marine invertebrates. Aquatic Microbial Ecology 38 (2005) 41-51
55. Leise E.M., Thavaradhara K., Durham N.R., and Turner B.E. Serotonin and nitric oxide regulate metamorphosis in the marine snail Ilyanassa obsoleta. American Zoologist 41 (2001) 258-267
56. Leise E.M., Kempf S.C., Durham N.R., and Gifondorwa D.J. Induction of metamorphosis in the marine gastropod Ilyanassa obsoleta: 5HT, NO and programmed cell death. Acta Biologica Hungarica 55 (2004) 293-300
57. Levantine P.L., and Bonar D.B. Metamorphosis of Ilyanassa obsoleta: Natural and artificial inducers. American Zoologist 26 (1986) 14A
58. Lin M.-F., and Leise E.M. Gangliogenesis in the prosobranch gastropod Ilyanassa obsoleta. Journal of Comparative Neurology 374 (1996) 180-193
59. Lucas C.H., Banham C., and Holligan P.M. Benthic-pelagic exchange of microalgae at a tidal flat. 2. Taxonomic analysis. Marine Ecology-Progress Series 212 (2001) 39-52
60. Matthews I., and Cook P.A. Diatom diet of abalone post-larvae (Haliotis midae) and the effect of pre-grazing the diatom overstorey. Marine and Freshwater Research 46 (1995) 545-548
61. McGee B.L., and Targett N.M. Larval habitat selection in Crepidula (L.) and its effect on adult distribution patterns. Journal of Experimental Marine Biology and Ecology 131 (1989) 195-214
62. McIntire C.D., and Amspoker M.C. Effects of sediment properties on benthic primary production in the Columbia River estuary. Aquatic Botany 24 (1986) 249-267
63. McIntyre H.L., Geider R.J., and Miller D.C. Microphytobenthos: the ecological role of the "secret garden" of unvegetated, shallow-water marine habitats. I. Distribution, abundance and primary production. Estuaries 19 (1996) 186-201
64. Morse A.N.C. How do planktonic larvae know where to settle?. American Scientist 79 (1991) 154-167
65. Morse D.E. Recent progress in larval settlement and metamorphosis: closing the gaps between molecular biology and ecology. Bulletin of Marine Science 46 (1990) 465-483
66. Najmudeen T.M., and Victor A.C.C. Seed production and juvenile rearing of the tropical abalone Haliotis varia Linnaeus 1758. Aquaculture 234 (2004) 277-292
67. Nasr D.H. Feeding and growth of the pearl oyster Pinctada margaritifera (L) in Dongonab Bay, Red-Sea. Hydrobiologia 110 (1984) 241-245
68. Nearhoof J.E. The Distribution and Relative Abundance of Benthic Microalgae and Phytoplankton in North Carolina Estuaries of Varying Depth and Clarity. Biology (1994), University of North Carolina Wilmington, Wilmington 52
69. Osorio R.C., Bustos P.V., and Bustos R.E. Gastric contents of the clam (Venus antigua antigua King and Broderip, 1835) in Ancud, Chile (Mollusca, Veneridae). Investigacion Pesquera (Santiago) 34 (1987) 139-147
70. Pastore M., Panetta P., Andreoli C., and dell Angelo B. Growth of Mytilus galloprovincialis Lamarck in the sea around Taranto. Oebalia 2 (1976) 20-61
71. Pechenik J.A. Growth and energy balance during the larval lives of three prosobranch gastropods. Journal of Experimental Marine Biology and Ecology 44 (1980) 1-28
72. Qian P.-Y., Thiyagarajan V., Lau S., and Cheung S. Relationship between bacterial community profile in biofilm and attachment of the acorn barnacle Balanus amphitrite. Aquatic Microbial Ecology 33 (2003) 225-237
73. Roberts R. A review of settlement cues for larval abalone (Haliotis spp.). Journal of Shellfish Research 20 (2001) 571-586
74. Roberts R.D., Kawamura T., and Nicholson C.M. Growth and survival of postlarval abalone (Haliotis iris) in relation to development and diatom diet. Journal of Shellfish Research 18 (1999) 243-250
75. Roberts R.D., Kawamura T., and Handley C.M. Factors affecting settlement of abalone (Haliotis iris) larvae on benthic diatom films. Journal of Shellfish Research 26 (2007) 323-334
76. Rodríguez S.R., Ojeda F.P., and Inestrosa N.C. Settlement of benthic marine invertebrates. Marine Ecology Progress Series 97 (1993) 193-207
77. Sakshaug E., and Holm-Hansen O. Chemical composition of Skeletonema costatum (Grev.) Cleve and Pavlova (Monochrysis) lutheri (Droop) green as a function of nitrate-, phosphate-, and iron-limited growth. Journal of Experimental Marine Biology and Ecology 29 (1977) 1-34
78. Sawatpeera S., Kruatrachue M., Sonchaeng P., Upatham S., and Rojanasarampkit T. Settlement and early growth of abalone larvae Haliotis asinina Linnaeus in response to the presence of diatoms. Veliger 47 (2004) 91-99
79. Scheltema R.S. The effect of substrate on the length of planktonic existence in Nassarius obsoletus. Biological Bulletin 111 (1956) 312
80. Scheltema R.S. Metamorphosis of the veliger larvae of Nassarius obsoletus (Gastropoda) in response to bottom sediment. Biological Bulletin 120 (1961) 92-109
81. Scheltema R.S. Pelagic larvae of New England intertidal gastropods I. Nassarius obsoletus Say and Nassarius vibex Say. Transactions of the American Microscopical Society 81 (1962) 1-11
82. Scheltema R.S. Environmental factors affecting length of pelagic larval development in the gastropod, Nassarius obsoletus. American Zoologist 2 (1962) 445
83. Scheltema R.S. Feeding habits and growth in the mud-snail Nassarius obsoletus. Chesapeake Science 5 (1964) 161-166
84. Smith D.L. A Guide to Marine Coastal Plankton and Marine Invertebrate Larvae (1977), Kendall/Hunt Publ. Co., Dubuque, IA 161 pp.
85. Sokal R.R., and Rohlf F.J. Biometry: The Principles and Practices of Statistics in Biological Research (1995), W.H. Freeman and Co., New York
86. Stein J.L. Handbook of Phycological Methods: Culture Methods and Growth Measurements (1973), Cambridge University Press, New York 448 pp.
87. Tamburri M.N., Zimmer-Faust R.K., and Tamplin M.L. Natural sources and properties of chemical inducers mediating settlement of oyster larvae: a re-examination. Biological Bulletin 183 (1992) 327-338
88. Tamburri M.N., Luckenbach M.W., Breitburg D.L., and Bonniwell S.M. Settlement of Crassostrea ariakensis larvae: effects of substrate, biofilms, sediment and adult chemical cues. Journal of Shellfish Research 27 (2008) 601-608
89. Thavaradhara K., and Leise E.M. Localization of nitric oxide synthase-like immunoreactivity in the developing nervous system of the snail Ilyanassa obsoleta. Journal of Neurocytology 30 (2001) 449-456
90. Walters L.J., Hadfield M.G., and Smith C.M. Waterborne chemical compounds in tropical macroalgae: positive and negative cues for larval settlement. Marine Biology 126 (1996) 383-393
91. Wethey D.S. Ranking of settlement cues by barnacle larvae: influence of surface contour. Bulletin of Marine Science 39 (1986) 393-400
92. Whiting M.C., and McIntire C.D. An investigation of distributional patterns in the diatom flora of Netarts Bay, Oregon, by correspondence analysis. Journal of Phycology 21 (1985) 655-661
93. Wieczorek S.K., and Todd C.D. Inhibition and facilitation of settlement of epifaunal marine invertebrate larvae by microbial biofilm cues. Biofouling 12 (1998) 81-118
94. Woodin S.A. Recruitment of infauna: positive or negative cues?. American Zoologist 31 (1991) 797-807
95. Woodin S.A., Marinelli R.L., and Lindsay S.M. Process-specific cues for recruitment in sedimentary environments: geochemical signals?. Journal of Marine Research 56 (1998) 535-558
96. Yang J. Observations on food of cumaceans and post larvae of mollusks in the Bohai Sea. Marine Science/Haiyang Kexue 6 (1998) 36-37
97. Zar J.H. Biostatistical Analysis (2010), Prentice-Hall, Inc., Upper-Saddle River, N.J. 944 pp.
98. Zhao B., and Qian P.-Y. Larval settlement and metamorphosis in the slipper limpet Crepidula onyx (Sowerby) in response to conspecific cues and the cues from biofilm. Journal of Experimental Marine Biology and Ecology 269 (2002) 39-51
99. Zimmer R., and Butman C. Chemical signaling processes in the marine environment. Biological Bulletin 198 (2000) 168-187