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Evidence for Sequential Hermaphroditism in Sabellastarte Spectabilis (Polychaeta: Sabellidae) in Hawai‘I1

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Evidence for Sequential Hermaphroditism in Sabellastarte Spectabilis (Polychaeta: Sabellidae) in Hawai‘I1 Evidence for Sequential Hermaphroditism in Sabellastarte spectabilis (Polychaeta: Sabellidae) in Hawai‘i1 David R. Bybee,2,4 Julie H. Bailey-Brock,2 and Clyde S. Tamaru3 Abstract: Understanding the reproductive characteristics of Sabellastarte specta- bilis (Grube, 1878), an economically important polychaete worm collected for the aquarium trade, is essential to the development of artificial propagation and conservation of coral reefs. The purpose of this study was to determine whether S. spectabilis is hermaphroditic. Using histological techniques, 180 indi- viduals were examined for gametes. Gametes were present only in abdominal segments. Primary oocytes were 7–8 mm in diameter in histologically prepared sections. Sperm appeared as round black dots about 2 mm in diameter on histo- logically prepared slides. Most individuals sampled had only one type of gamete in the coelom, but both eggs and sperm were seen in the coelom of 15% of individuals, demonstrating the occurrence of hermaphroditism in Hawaiian populations of S. spectabilis. The sex ratio of males to females was skewed signif- icantly toward males in both the small (6–8 mm diameter) and medium (9–10 mm diameter) sized worms. Among the largest worms (11–13 mm diameter), the sex ratio did not diverge significantly from 1:1. There was a significantly higher proportion of hermaphrodites (30%) in the large size class. Worms of unknown gender, although present in all size classes examined, were most fre- quent (33%) in the medium size class. These patterns are consistent with se- quential (protandrous) hermaphroditism. The sabellid polychaete Sabellastarte pal collection site for this commercially im- spectabilis (Grube, 1878) is common in bays portant ornamental species (Walsh et al. and harbors in the main Hawaiian Islands 2003). These worms settle in cracks and and particularly in Ka¯ne‘ohe Bay, on the crevices of living and dead reef corals, mak- windward coast of O‘ahu. Ka¯ne‘ohe Bay is ing collection difficult and damaging to the partially cut off from the ocean by a barrier reef community. Reproduction is currently reef, which protects it from large waves being studied in this species (Bybee et al. in and provides an ideal habitat for these soft- press) with the goal of facilitating artificial tubed filter feeders. Sabellastarte spectabilis is propagation to reduce pressure on coral reefs very abundant in the bay, which is the princi- due to destructive collecting practices. 1 The PADI Foundation, the Edmondson Fund (Uni- from the NOAA Office of Sea Grant, U.S. Department versity of Hawai‘i), and The Center for Tropical and of Commerce, and the State of Hawai‘i Department of Subtropical Aquaculture provided financial support for Agriculture, Aquaculture Development Program, Con- this project. This paper is funded in part by grants/ tracts No. 49855 and 52663. The views expressed herein cooperative agreements from the U.S. Department of are those of the authors and do not necessarily reflect the Agriculture, CSREES Agreement No. 2002-38500- views of NOAA, USDA, the State of Hawai‘i, or any of 12039; National Oceanic and Atmospheric Administra- their subagencies. UNIHI-SEAGRANT-JC-04-09. Fa- tion, Project No. A/AS-1, which is sponsored by the cilities were generously made available for this research University of Hawai‘i Sea Grant College Program, at the Hawai‘i Institute of Marine Biology (contribution SOEST, under Institutional Grant No. NA16RG2254 no. 1216). Manuscript accepted 9 December 2005. 2 Department of Zoology, University of Hawai‘i at Ma¯noa, Honolulu, Hawai‘i. 3 College Sea Grant Program, University of Hawai‘i Pacific Science (2006), vol. 60, no. 4:541–547 at Ma¯noa, Honolulu, Hawai‘i. : 2006 by University of Hawai‘i Press 4 Corresponding author (fax: 808-956-9812; e-mail: All rights reserved [email protected]). 541 542 PACIFIC SCIENCE . October 2006 Polychaetes are predominately gonochoric ditic and the nature of the hermaphroditism (separate sexes) (Schroeder and Hermans formed the basis for this investigation. 1975) with hermaphroditism occurring in a minority of families. Of the 9,000 known materials and methods species belonging to 81 families of polychaetes (Rouse and Pleijel 2001), hermaphroditism Worms were collected at monthly intervals has been reported in a total of 67 species (2002–2003) from the reefs surrounding the among 25 families (Giangrande 1997). About Hawai‘i Institute of Marine Biology on Moku half of the reported hermaphroditic species O Lo‘e (also known as Coconut Island) in are sequential hermaphrodites (36); the ma- Ka¯ne‘ohe Bay for histological analyses of ga- jority of those (32) are protandrous forms metogenesis and examination of their inter- (Giangrande 1997). The remainder (31) are nal anatomy. Whole specimens were fixed in simultaneous hermaphrodites (Schroeder and 10% seawater formalin for a minimum of 72 Hermans 1975, Giangrande 1997). hr, after which they were transferred to 80% Gonochorism is also the predominant con- ethanol for long-term storage. Transverse dition within the Sabellidae, though her- sections were taken from both the thorax maphroditism is not uncommon. Most of the and abdomen of whole worms. Tissue sam- reported sabellid hermaphrodites are listed ples were placed in tissue cassettes and were as simultaneous, and sequential (protandrous) then processed using a tissue processor (Shan- forms seem to be rare (Rouse and Fitzhugh don Citadel 2000) and embedded in paraplast 1994). However, it has been hypothesized with an embedding center (Tissue Tek III). that sequential hermaphroditism is probably The paraplast blocks were sectioned at a more widespread than we know and that thickness of 4 mm using a microtome (Ameri- more detailed studies are needed to sup- can Optical) and placed on microscope slides. port this supposition (Rouse and Fitzhugh The slides with adhered sections were then 1994). cleared with xylene and dehydrated through There are eight accepted species in the an alcohol series and finally stained with genus Sabellastarte according to the most hematoxylin/eosin stain. Individuals were recent revision (Knight-Jones and Mackie classified as male if only sperm were present 2003). Of those eight species, only two have and female if only oocytes were found. Those any published information on reproductive with both male and female gametes were clas- mode. Runganathan (1943) observed S. mag- sified as hermaphrodites. Worms with only nifica (Shaw, 1800) [later identified as S. indica coelomocytes were classified as unknown. (Savigny, 1822)] (Rouse and Fitzhugh 1994) Fresh samples of coelomic contents were also to be a simultaneous hermaphrodite. Sabellas- extracted from live worms, and gametes were tarte indica has since been synonymized with digitally photographed using a compound S. spectabilis (Knight-Jones and Mackie 2003). light microscope (Nikon Eclipse E200). Rouse and Fitzhugh (1994) observed three The body diameter of worms (removed preserved specimens of the same species, two from tubes) collected during months in which ‘‘small’’ individuals from Kiribati and one gametogenesis is known to occur (May– from Palau (Belau). All three were reportedly November) was measured with calipers to gonochoric. They also examined two pre- the nearest millimeter, and worms were di- served specimens of S. magnifica. One speci- vided into three different size classes (small, men (from the West Indies) was found to be 6–8 mm; medium, 9–10 mm; and large, 11– a simultaneous hermaphrodite and the other 13 mm). Worms were further placed into the (from Puerto Rico) was gonochoric. Under- following reproductive groups: male, female, standing the reproductive characteristics of S. hermaphrodite, and unknown, based on ob- spectabilis, an economically important worm, servations made from the histologically pre- is a prelude to the development of means to pared slides. A chi square (X 2) test was used artificially propagate the species. Determining to assess the statistical significance of various whether or not this polychaete is hermaphro- levels of abundance between groups. Sequential Hermaphroditism in Sabellastarte spectabilis . Bybee et al. 543 Scanning Electron Microscopy 1D). A more detailed description of S. specta- bilis larval morphology and discussion of life Scanning electron microscopy (SEM) was history implications is found in Bybee et al. used to confirm spermatocytes. This was (in press). For a review of polychaete sperma- done by first extracting coelomic contents tozoa morphology see Jamieson and Rouse from several individuals until a male was (1989). found. The contents were pipetted from the Most worms (85%) had only one type of coelom, then fixed with 4% gluteraldehyde gamete in the coelom and were designated in 0.1 molar sodium cacodylate buffer (7.6) as being male or female. Several individuals with 0.35 molar sucrose. They were washed (15%) clearly possessed both oocytes and in 0.1 molar sodium cacodylate buffer with spermatocytes (Figure 1A,B) and were classi- 0.44 molar sucrose. Coelomic contents were fied as hermaphrodites (Table 1). Individuals then postfixed with 1% osmium tetroxide in in which no gametes could be identified were buffer and dehydrated in a graded series of classified as unknown. Observations of coelo- ethanol, critical point dried, and mounted mic contents of live worms were consistent on aluminum stubs. They were then sputter with histological observations. A histogram coated with gold palladium and viewed in a (Figure 2) revealed that the sex ratio of males field emission scanning electron microscope to females was skewed significantly toward (Hitatchi S-800) at 15 kv accelerating voltage. males (P < 0:01, X 2 test) in both the small The abdomen and thorax were also sectioned and medium size classes. In the large size and prepared for histological processing as class, however, the sex ratio did not diverge just described. significantly from 1:1. The proportion of hermaphrodites found in the large size class 2 results was significantly higher (P < 0:05, X test) than what was observed in the small and me- To date, gender in S.
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