Abstract
The sabellid polychaete Sabellastarte spectabilis (Grube 1878) was collected at approximately monthly intervals from January 2002 to December 2003 from intertidal and subtidal reefs near the Hawaii Institute of Marine Biology in Kane’ohe Bay, Hawaii, USA (21°N, 157°W). Gametogenesis and spawning periodicity were investigated using histological techniques and induction of spawning trials. Worms were characterized into four discrete reproductive stages based on histological evidence: (1) No evidence of reproductive activity in the coelom (sex cannot be determined), (2) Only coelomocytes present in the coelom (sex cannot be determined), (3) Some gametes present in the coelom (sex can be determined) and (4) Coelom densely packed with gametes (sex can be determined). The small hermaphroditic portion of the population was not used in this study. Stage 4 worms were present over an extended period of time (females, March–December and males, March–November) indicating a potentially broad reproductive season. No correlation between day length and maturation stages in S. spectabilis was detected. However, the statistical model Y = ([394.26 × X] − [7.793 × X2]) − 4960.781 where Y the % frequency of Stage 4 worms and X the mean monthly water temperature explained 44% of the variation between water temperature and % frequency of Stage 4 worms. Maturation appeared to coincide with water temperatures of 24–25°C (March–September) after which there is a reduction in the % frequency of stage 4 individuals. Induction of spawning trials conducted between May and January showed the month of October with a significantly higher percent success than any other month investigated. According to all available information (e.g., natural spawning in water tables, histological data, induction of spawning trials, correlation of maturation stages with observed changes in average monthly water temperature.), there is an apparent peak in reproductive activity (spawning) within a broad maturational season, which may be influenced by water temperature.
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References
Bailey-Brock JH (1987) Phylum Annelida. In: Devaney DM, Eldredge LG (eds) Reef and shore fauna of Hawaii. Bishop Museum Press, Honolulu, Hawaii
Bentley MG, Boyle J, Pacey A (1994) Environmental influences on endocrine systems controlling reproduction in polychaetes. Mem Mus Natl Hist Nat 162:30–37
Bybee DR, Bailey-Brock JH, Tamaru CS (2006a) Larval Development of the fanworm Sabellastarte spectabilis in Hawaiian Waters. Sci Mar 60:541–547
Bybee DR, Bailey-Brock JH, Tamaru CS (2006b) Evidence for sequential hermaphroditism in Sabellastarte spectabilis (Grube 1878) (Polychaeta: Sabellidae). Pac Sci 60:541–547
Cotter ER, O’Riordan M, Meyers AA (2003) A histological study of reproduction in the serpulids Pomatoceros triqueter and Pomatoceros lamarckii (Annelida: Polychaeta). Mar Biol 142:905–914
Currie DR, McArthur MA, Cohen BF (2000) Reproduction and distribution of the invasive European fanworm Sabella spallanzanii (Polychaeta: Sabellidae) in Port Phillip Bay, Victoria, Australia. Mar Biol 136:645–656
Dales RP (1961) The coelom and peritoneal cell systems of the sabellid polychaetes. Q J microsc Sci 102:327–346
Dean SR, Chapman M, Chapman CS (1987) Reproduction and development of the sabellid polychaete Myxicola infundibulum. J Mar Biol Assoc UK 67:431–439
Durkina VB, Garkusha AA (2000) Oogenesis in the polychaete Dipolydora commensalis. Russ J Mar Biol 26:439–444
Eckelbarger KJ (1979) Ultrastructural evidence for both autosynthetic and heterosynthetic yolk formation in the oocytes of an annelid (Phragmatopoma lapidosa: Polychaeta). Tissue Cell 11:425–443
Eckelbarger KJ (1983) Evolutionary radiation in polychaete ovaries and vitellogenic mechanisms; their possible role in life history patterns. Can J Zool 61:487–504
Eckelbarger KJ (1984) Comparative aspects of oogenesis in polychaetes. In: Fisher A, Pfannenstiel HD (eds) Polychaete reproduction: progress in comparative reproductive biology. Gustav Fischer Verlag, New York
Eckelbarger KJ (1988) XVI. Oogenesis and female gametes. In: Westheide W, Hermans CO (eds) The ultrastructure of the Polychaeta, vol. 4, Microfauna Marina. Gustav Fischer Verlag, New York
Eckelbarger KJ (1992) Polychaete oogenesis, In: Harrison FW, Gardiner SL (eds) Microscopic anatomy of invertebrates, vol. 7, Annelida. Wiley-Liss, New York
Eckelbarger KJ, Grassle JP (1982) Ultrastructure of the ovary and oogenesis in the polychaete Capitella jonesi (Hartman 1959). J Morphol 171:305–320
Eckelbarger KJ, Young CM, Ramirez L, Brooke S, Tyler P (2001) Gametogenesis, spawning behavior, and early development in the “iceworm” Hesiocaeca methanicola (Polychaeta: Hesionidae) from methane hydrates in the Gulf of Mexico. Mar Biol 138:761–775
Fitzhugh K (1989) A systematic revision of the Sabellidae-Caobangiidae-Sabellongidae complex (Annelid: Polychaeta). Bull Amer Mus Nat Hist no. 192, New York.
Gambi MC, Patti FP (1999) Reproductive biology of Perkinsiana antarctica (Kinberg) (Polychaeta, Sabellidae) in the Straits of Magellan (South America): systematic and ecological implications. Sci Mar 63:253–259
Giangrande AM (1997) Polychaete reproduction patterns life cycles and life histories: an overview. Oceangr Mar Biol Annu Rev 35:323–386
Giangrande AM, Licciano P, Pagliara Gambi MC (2000) Gametogenesis and larval development in Sabella spallanzanii (Polychaeta: Sabellidae) from the Mediterranean Sea. Mar Biol 136:847–861
Hsieh HL (1997) Self fertilization—a potential fertilization mode in an estuarine sabellid polychaete. Mar Ecol Prog Ser 147:143–148
Jokiel PL, Brown EB (2004) Global warming, regional trends and inshore environmental conditions influence coral bleaching in Hawaii. Global Change Biol 10:1627–1641
Knight-Jones P, Bowden N (1984) Incubation and scissiparity in Sabellidae (Polychaeta). J Mar Biol Assoc UK 64:809–818
Knight-Jones P, Mackie ASY (2003) A revision of Sabellastarte (Polychaeta: Sabellidae). J Nat Hist 19:2269–2301
Kupriyanova EK, Nish E, Ten Hove HA, Rzhavsky AV (2001) Life-history patterns in serpulimorph polychaetes: ecological and evolutionary perpectives. Oceanogr Mar Biol Annu Rev 39:1–101
Licciano M, Giangrande A, Gambi MC (2002) Reproduction and simultaneous Hermaphroditism in Branchiomma luctuosum (Polychaeta, Sabellidae) from the Mediterranean Sea. Invert Biol 121:55–65
McEuen FS, Wu BL, Chia FS 1983 Reproduction and development of Sabella media, a sabellid polychaete with extratubular brooding. Mar Biol 76:301–309
Nash R, Keegan BF (2003) Reproductive cycle of Bispira volutacornis (Polychaeta: Sabellidae) on the west coast of Ireland. Mar Biol 143:919–925
Olive PJW (1984) Environmental control of reproduction in Polychaeta. Fortschr Zool 29:17–38
Olive PJW (1995) Annual breeding cycles in marine invertebrates and environmental temperature: probing the proximate and ultimate causes of reproductive synchrony. J Therm Biol 20:79–90
Olive PJW, Clark RB (1978) Physiology of reproduction. In: Mill PJ (ed) Physiology of annelids. Academic, New York
Patti FP, Gambi MC, Giangrande A (2003) Preliminary study on the systematic relationships of Sabellinae (Polychaeta, Sabellidae), based on the C1 domain of the 28S rDNA, with discussion of reproductive features. Ital J Zool 70:269–278
Rice SA (1992) Polychaeta: Spermatogenesis and spermiogenesis. In: Harrison FW, Gardiner SL (eds), Microscopic anatomy of invertebrates. vol. 7, Annelida. Wiley-Liss, New York
Rouse GW (1999) Polychaeta, including Pogonophora and Myzostomida. In: Adiyodi, KG, Adiyodi RG (series eds) Reproductive biology of invertebrates, vol. 9 In: Jamieson B B B M (ed) Progress in male gamete ultrastructure and phylogeny, vol. IX, part B. Oxford and IBH Publishing, Calcutta
Rouse GW, Fitzhugh K (1994) Broadcast fables: is external fertilization really primitive: Sex, size and larvae in sabellid polychaetes. Zool Scripta 23:273–301
Rouse GW, Gambi MC (1998) Evolution of reproductive features and larval development in the genus Amphiglena (Polychaeta: Sabellidae). Mar Biol 131:743–753
Rouse GW, Jamieson BGM (1987) An ultrastructural study of the spermatozoa of the polychaetes Eurythoe complanata (Amphinomidae), Clymenella sp. And Micromaldane sp. (Maldanidae), with definition of sperm types in relation to reproductive biology. J Submicrosc Cytol 19:573–584
Rouse GW, Pleijel F (2001) Polychaetes. Oxford, New York
Rouse GW, Kupriyanova E, Nishi E (2006) Sabellida. In: Rouse G, Pliejel F (eds) Reproductive biology and phylogeny of Annelida, Chapter 12. Science Publishers, Enfield
Rousset V, Rouse GW, Siddall ME, Tillier A, Pleijel F (2004) The phylogenetic position of Siboglinidae (Anellida) inferred from 18S rRNA, 28S rRNA and morphological data. Cladistics 20:518–533
Schroeder PC, Hermans CO (1975) Annelida: Polychaeta. In: Geise AC, Pearse JS (eds) Reproduction of marine invertebrates. Academic, New York
Snedecor GW, Cochran WG (1967) Statiscal methods, 6th edn. Iowa State University Press, Ames
Walsh WJ, Cotton SP, Dierking J, Williams ID (2003) The commercial marine aquarium fishery in Hawai’i 1976–2003. In: Friedlander AM (ed) Status of Hawai’i’s coastal fisheries in the new millennium. Proceedings of a Symposium sponsored by the American Fisheries Society, Hawai’i chapter. Honolulu, Hawai’i
Wilson WH (1991) Sexual reproductive modes in polychaetes: classification and diversity. Bull Mar Sci 48:500–516
Acknowledgments
We are most grateful to Ron Shimojo and Lei Yamasaki at Anuenue Fisheries, Honolulu, for assistance with the histology. We thank Dr. Kevin Eckelbarger for advice on gametogenesis in polychaetes. We are also grateful to the PADI Foundation, the Edmondson Fund (University of Hawaii) and The Center for Tropical and Subtropical Aquaculture for financial support as well as the Hawaii Institute of Marine Biology (contribution #1241) for the use of their facilities. This research is funded in part by grants/cooperative agreements from the Center for Tropical and Subtropical > Aquaculture through Grant No. #2002-38500-12039 from USDA/CSREES. National Oceanic and Atmospheric Administration, Project # A/AS-1, which is sponsored by the University of Hawai’i Sea Grant College Program, SOEST, under Institutional Grant No. NA16RG2254 from the NOAA Office of Sea Grant, US Department of Commerce and the State of Hawaii Department of Agriculture, Aquaculture Development Program, Contracts No. 49855 and 52663. The views expressed herein are those of the authors and do not necessarily reflect the views of NOAA, USDA, State of Hawai’i or any of their sub-agencies. UNIHI-SEAGRANT-JC-04-09. All experiments herein comply with the current laws of the USA.
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Communicated by J.P. Grassle, New Brunswick.
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Bybee, D.R., Bailey-Brock, J.H. & Tamaru, C.S. Gametogenesis and spawning periodicity in the fan worm Sabellastarte spectabilis (Polychaeta: Sabellidae). Mar Biol 151, 639–648 (2007). https://doi.org/10.1007/s00227-006-0504-0
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DOI: https://doi.org/10.1007/s00227-006-0504-0