付 着 生 物 研 究 Marine Fouling 10 (1) 11-16, 1993

Notes on Reproductive Biology of Some Serpulid at Sesoko Island, Okinawa, with Brief Accounts of Setal Morphology of Three of and Filograna implexa

Eijiroh NISHI Amakusa Marine BiologicalLaboratory, Kyushu University, Tomioka, Amakusa, Kumamoto863-25 (ReceivedOctober 19, 1992)

Abstract: On the vertical walls of an aquarium and shells of Streptopinna saccata, 20 serpulid species were observed. Among them, 7 species perform brooding, 7 did . Brooding was separated into 3 types, branchial-brooding, brood pouch-incubation and tube incubation. Asexual reproduction of them is terminal and single, bud completes their external morphology within 5 to 8 days. Descriptions of specialized collar setae of Filograna implexa and 3 species of Salmacina were given.

The ecoiogy of serpulid species is well known used in the observations of , partic- in some fouling species (WISELY, 1956; ARA- ularly on setal morphology (e. g., EYBINE- KAWA, 1973; ARAKAWA and KUBOTA, 1973; JACOBSEN, 1991), among the genera Salmacina ABBOTT and REISH, 1980; MIURA and KAJIHARA, and Filograna, only KNIGHT-JONES (1981) ob- 1981). Among ecological characteristics, dis- served collar setae of Filograna implexa with tribution, reproduction and larval ecology were scanning electron microscope in my knowledge. well studied. Most serpulid species show Thus I observed collar setal morphology, which separate sexes and their larvae are plank- usually available in identification of the totrophic, others brood lecithotrophic larvae in Salmacina, using scanning electron microscope. various ways (TEN HOVE, 1979; BEN-ELIAHU Then I found notable difference among 3 Sal- and TEN HOVE, 1989; NISHI, 1992; NISHI and macina species and Filograna implexa. YAMASU, 1992 a, b, c). In this paper, setal morphology of the genera Filograna implexa and are Salmacina and Filograna were reported briefly, well known to distribute all over the world and compared to other related species. After- (ALLEN, 1953) and to brood embryos (FAULKNER, that, I noted notable reproductive characteristics, 1930). However, their has been very particularly brooding of embryos and asexual confused (e.g., GEE, 1963; SOUTHWARD, 1965). reproduction. Within the genera Salmacina and Filograna, Material and Methods collar setal morphology, number of thorax segments, number of branchial crowns, and Serpulid worms were collected from various morphology of pseudo-opercula are used in substrates in an aquarium at Sesoko Marine species identification (FAULKNER, 1930; GEE, Science Center, University of the Ryukyus, 1964; GALLARDO, 1967). But the detailed from October 1990 to February 1992. morphological and taxonomical studies are scat- Specimens were fixed by 10% glutar-aldehyde tered up to now. and dehydrated in a series of alcohol. For In Japan, OKUDA (1937) firstly reported the electron microscope observations (Hitachi S- occurrence of Salmacina dysteri, and later 530), they were dried using liquid CO2 and Uchida (1978) re-described Filograna implexa. coated with gold-palladium. Recently scanning electron microscope was well 12 Eijiroh NISHI

reached 23/tube (N=30). Results Paraprotis dendrova also frequently occurred Substratum and occurring species on vertical concrete walls of aquarium, their Totally 20 species of serpulids occurred in density varied 1-20/100cm2 (N=25). Colonies the aquarium (Table 1). Among them, Hydro- of S. tribranchiata were massive andwere ob- ides elegans, Josephella marenzelleri, Rhodopsis served on various substrates, mainly on mol- pusilla, Salmacina amphidentata, and Salmacina luscan shell and on algae. Fenestrated massive tribranchiata were abundant. elegans colonies of F. implexa rarely appeared on the frequently attached to the vertical walls of shell of S. saccata and on fouling plates. aquarium, their density reached commonly>50/ Pomatostegus stellatus and Vermiliopsis infundi- m2. On the tubes of H. elegans, J. marenzel- burum were solitary and sparsely distributed on leri and R. pusilla frequently settled, when they vertical concrete walls and on natural rocks. occurred on H. elegans tube, maximum density Protula tubularia rarely occurred on concrete

Table 1. Serpulid species occurred on concrete walls, molluscan shells, algae and artificial materials. Abundance is expressed by ++ (abundant), +(common), -(rare), -- (very rare). Abbreviations for substrate, Cw, concrete walls, Ss, Streptopinna saccata (bivalvia); Al, algae; Nr, natural rock; V, vinyls; Ca, cage; Pl, vinyl plate.

Table 2. Number and size of teeth, and width of notch on basal part of specialized col- lar setae (average±S. D.) from 3 to 4 worms in three species of Salmacina and Filograna

implexa. Notes on Reproductive Biology of Some Serpulid Polychaetes at Sesoko Island 13

Fig. 1. Procedure of asexual reproduction in Salmacina dysteri. A, appearance of branchial rudiments: B, 1 day later; C, 2 days later; D, 4 days later, appearance of thoracic membrane. m, thoracic membrane: r, rudiment of branchial crown.

blocks abundantly, maximum density reached Reproductive biology 25/100cm2. Among 20 serpulid species, 7 species perform Collar setal morphology brooding. Their brooding could be separated Number and size of teeth on basal part and into following 3 types; branchial brooding in width of notch on specialized collar setae in Paraprotis dendrova, brood-pouch incubation in three species of Salmacina and Filograna implexa R. pusilla, and tube incubation in F. implexa are shown in Table 2. Generally teeth size of and 3 species of Salmacina. Among them, F. implexa were gradually decreased toward except for R. pusilla, brooding was not con- their base. That of S. amphidentata had many firmed in field because they brood embryos long heavy teeth (Fig. 2). The tooth distribu- within calcareous tube. Rhodopsis pusilla had tion pattern of S. amphidentata, S. dysteri and some calcareous brood pouches attached above S. tribranchiata were similar to each other. growth line of tube wall, thus it was easy to The setae of S. amphidentata have most wide identify only their tubes if the brood pouch notch, S. tribranchiata and S. dysteri have a occurred, even on naked eyes. notch about 5μm width (Table 2). The notch Filograna implexa, 3 species of Salmacina, of setae in F. implexa was very short, about J. marenzelleri and R. pusilla commonly ex- 3μm length (Table 2). Intra-specific collar setal hibited asexual reproduction as shown in Fig. variation was not observed in this study. 1. Most processes of asexual reproduction 14 Eijiroh NISHI

other aperture. All the asexually reproducing species were able to be employed both types, Josephella marenzelleri and Rhodopsis pusilla usually exhibited dispersive one, three species of Salmacina and Filograna implexa frequently did non-dispersive one.

Discussion UCHIDA (1978) studied Filograna implexa at Wakayama, Japan, suggested that Salmacina amphidentata is a synonym of F. implexa, be- cause he thought newly budded-off worm have incomplete collar setae and JONES (1962) de- scribed them. However JONES noted they Fig. 2. Specialized collar setae in 4 serpulid might be brooded embryos, some worms were species. A, Filograna implexa; B, Salmacina considered to be mature. And newly budded tribranchiata; C, Salmacina dysteri; D, worms had similar collar setae to the adult Salmacina amphidentata. one when they released in S. dysteri and F. implexa (NISHI, unpulished). In addition, their were same in these 6 species, but the position collar setal morphology is significantly different of bud appeared on the adult abdomen and a (Fig. 3 and Table 2) in adult stage between S. period for the complement of buds was dif- dysteri and S. amphidentata. Thus I considered, erent. Salmacina and Filograna, usually had S. amphidentata is not a synonym of other 12-26 abdominal segments, a bud appeared species. between anterior 3 to 10 abdominal segments. Although this study treated only the collar Adults of R. pusilla and J. marenzelleri had setal morphology to separate related species, usually 10 to 16 abdominal segments, then a other morphological and ecological characters bud appeared between 2 to 5 anterior segments. might be available for the classification of The bud developed into an individual worm Salmacina species. For example, approaching (Fig. 1), within 5 days in R. pusilla and J. serpulid taxonomy, recently EKARATNE et al. marenzelleri, and within 7 or 8 days in F. (1982) used starch-gel electrophoresis to separate implexa and Salmacina spp. The bud grew 2 species of Pomatoceros, and TEN HOVE and until they become similar to adult in size and PANTUS (1985) suggested blood vessel pattern in morphology attained. Then they become may be useful in the taxonomy of Apomatus- separated from the stock, later a new branch Protula complex. of tube arose. TEN HOVE (1979) suggested that following New tube production was separated into two factors are important in the process of colony cases, dispersive without connection between formation or aggregation in serpulid poly- bud and stock worm and non-dispersive one chaetes; physical conditions, asexual reproduc- with their connection. Dispersive bud-tube is tion, brooding of embryos, gregariousness of extended from the mouth of tube, and reached larvae. In aggregating species occurring in the to another substratum. This type is usually aquarium, brooding also seems likely very thin more than adult one. Non-dispersive one important. In fact, 7 species out of 20 species is formed from the collar like portion which are brood their larvae (Table 1). Their larvae is oval and slightly wider than the rest of the did not disperse far away, and showed weak tube. Next a partition is built dividing the gregariousness during settlement (NISHI, un- oval aperture into two and the parent worm published), thus dense conspecific aggregation continues tube-formation through one aperture is facilitated, as well as asexual reproduction. while the individual that has been budded off Asexually reproducing or brooding serpulids communicates with the exterior through the observed in an aquarium are not common in Notes on Reproductive Biology of Some Serpulid Polychaetes at Sesoko Island 15

coral reef area, only 3 species (Salmacina dysteri, known but widely distributed species of Ser- S. amphidentata, Paraprotis dendrova) were pulidae (Polychaeta). Zool. Sci., 18, 381-385. commonly found among 45 serpulid species EIBYE-JACOBSEN, D. (1991). Observations on setal sampled from the nearshore of Sesoko Island morphology in the Phyllodocidae (Polychaeta: Annelida), with some taxonomic considerations. (NISHI, unpublished). Josephella marenzelleri Bull. Mar. Sci., 48, 530-543. and R. pusilla could not find outside the EKARATNE, K. A., H. BURFITT, M. W. FLOWERDEW aquarium during careful observation (NISHI, and D. J. CRISP (1982). Separation of the two unpublished). Probably they migrated from Atlantic species of Pomatoceros, P. lamarckii competitively complicated area such as coral and P. triqueter (Annelida, ) by reefs, and are now distributed mainly on means of biochemical genetics. Mar. Biol., artificial substrata. On artificial substrata, 71, 257-264. competition may be less severe, but the in- FAULKNER, G. H. (1930). The anatomy and the troduction of these substrates may be op- histology of bud-formation in the serpulid portunistic. Thus they reproduce more rapidly Filograna implexa, together with some cyto- than other species and predominated on op- logical observations on the nuclei of the neo- blasts. J. Linn. Soc., London, 37, 109-190. portunistic substrate. GALLARDO, V. A. (1967). Description of Salmacina Acknowledgements chilensis n. sp. (Polychaeta, Serpulidae) from Northern Chile. Boln Soc. Biol. Conception, I would like to thank Dr. T. KIKUCHI, 41, 9-12. Kyushu University, Dr. T. MIURA, Kagoshima GEE, J. M. (1963). On the taxonomy and distribu- University, and Dr. T. YAMASU, University of tion in South Wales of Filograna, Hydroides the Ryukyus, for their useful suggestions and and Mercierella (Polychaeta: Serpulidae). Ann. for critically reading the manuscript. I thank Mag. Nat. Hist., 6, 705-715. also to Dr. C. H. THORP, Portsmouth Poly- TEN HOVE, H. A. (1979). Different causes of mass occurrence in serpulids. In: Biology and sys- technic, for his careful reading the draft of tematics of colonial organisms (ed. by G. this manuscript. LARWOOD and B. R. ROSEN), pp. 281-298, Acade- References mic Press, London and New York. TEN HOVE, H. A. and J. A. PANTUS (1985). Dis- ABBOTT, D. P. and D. J. REISH (1980). Polychaeta: tinguishing the genera Apomatus Philipi, 1884 The marine worms. In: Intertidal in- and Protula Risso, 1826 (Polychaeta: Ser- vertebrates of California, (ed. by R. H. MORRIS, pulidae). A further plea for a methodological D. P. ABBOTT, and E. C. HADERLIE), pp. 448- approach to serpulid taxonomy. Zool. Meded., 489, Stanford University Press, California. 59, 419-437. ALLEN, F. E. (1953). Distribution of marine in- HUXLEY, T. A. (1855). On a hermaphrodite and vertebrates by ships. Aust. J. Mar. Freshw. fissiparous species of tubicolous annelid. Edin- Res., 4, 307-316. burgh new Phil. J., 1, 113-143. ARAKAWA, Y. (1973). Biological studies on pre- JONES, M. L. (1962). On some polychaetous an- vention and extermination of fouling organisms nelids from Jamaica, the West Indies. Bull. attached to cultured oysters, 2. Early life Am. Mus. Nat. Hist., 124, 171-212. history of (Polychaeta: KNIGHT-JONES, P. (1981). Behavior, setal inversion Annelida). Bull. Hiroshima Fish. Exp. St., 4, and phylogeny of the (Polychaeta). 19-27. (in Japanese with English abstract). Zool. Sci., 10, 183-202. ARAKAWA, Y. and H. KUBOTA (1973). Biological MIURA, T. and T. KAJIHARA (1981). The develop- studies on prevention and extermination of ment of a serpulid worm Hydroides ezoensis fouling organisms attached to cultured oysters, (Annelida, Polychaeta). Proc. Jap. Soc. Syst. 1. Distribution and seasonal settlement of Zool., 20, 7-20. Hydroides norvegica (Polychaeta: Annelida) NISHI, E. (1992). Occurrence of coral boring ser- in Hiroshima Bay. Bull. Hiroshima Fish. Exp. pulid Floriprotis sabiuraensis Uchida and brood- St., 4, 13-17. (in Japanese with English ab- ing serpulid Paraprotis dendrova Uchida at stract). Okinawa. Galaxea, 11, 15-20. BEN-ELIAHU, M. N. and H. A. TEN HOVE (1989). NISHI, E. and T. YAMASU (1992a). Brooding and Redescription of Rhodopsis pusilla Bush, a little development of a serpulid tube worm Salmacina 16 Eijiroh NISHI

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