BULLETIN OF MARINE SCffiNCE, 27(2): 241-255, 1977
LARVAL DEVELOPMENT OF SA BELLA RIA FLORIDENSIS FROM FLORIDA AND PHRAGMATOPOMA CALIFORNICA FROM SOUTHERN CALIFORNIA (POLYCHAETA : SABELLARIIDAE), WITH A KEY TO THE SABELLARIID LARVAE OF FLORIDA AND A REVIEW OF DEVELOPMENT IN THE FAMIL Y
Kevin J. Eckelbarger
ABSTRACT A laboratory study was conducted on the larval development, metamorphosis, and settlement behavior of Sabella ria floridensis from Florida, with additional observations on the development of Pllragmatopoma californica from California. Metamorphosis of S. floridensis larvae occurred 18 to 27 days from fertilization at 2l-23°C with many larvae metamorphosing in the absence of sand grains or other substrate. Metamorphosis was followed by a crawling or exploratory period ranging from several hours to several days before larvae constructed tubes and began a sedentary existence. The significance of this unusual behavior is discussed and compared to that of other sabellariids. A summary of systematically-useful larval characters for the identification of sabellariid larvae, a key to the sabellariid larvae of Florida and a comparison of larval development times within the family are presented.
Information on the larval development of planktologist to make specific identifications eight species of sabellariids has appeared of sabellariid larvae from plankton samples. previously. These include three European This paper presents a comparison of larval species: Sabel/aria alveolata (Linne) (Wil- development times in sabellariids, a summary son, 1929, 1968a, 1970a; Cazaux, 1964); of systematically useful larval characters and Sabellaria spinulosa Leuckart (Wilson, 1929, a key to the sabeJlariid larvae of Florida. 1970b) and Lygdamis muratus (Allen) (Wilson, 1929; Bhaud, 1969, 1975a); two 'MATERIALS AND METHODS species from the east coast of North America: Sabellaria vulgaris Verrill (Novikoff, 1957; For the studies of larval development of Curtis, 1973; Eckelbarger, 1975) and Sabellaria floridensis, specimens were ob- Phragmatopoma lapidosa Kinberg (Mauro, tained in August 1974 from the Gulf Speci- 1975; Eckelbarger, 1976); a single species men Company Inc. The worms were col- from California: Phragmatopoma californica lected in the Apalachee Bay area, Wakulla (Fewkes) (Hartman, 1944; Dales, 1952); County, Florida. Spawning, handling and and a single species from the Indian Ocean: maintenance of eggs and larvae were carried Lygdamis indicus Kinberg (Bhaud, 1975b). out according to the procedures described by The present paper deals with an additional Eckelbarger (1975). The larvae were main- sabellariid from Florida, Sabel/aria floridensis tained at room temperature (21-23°C) in Hartman, as well as additional observations circulating sea water of the same salinity on Phragmatopoma californica from Cali- (25%0) in which the adults were collected. fornia. Drawings of paleae and spines were made Previous studies of larval development in by preparing whole-mounts of the larvae on sabellariids have demonstrated great similar- microscope slides and photographing them ities in larval morphology between the species with Kodachrome II color slide film through studied, thus making it difficult for the zoo- a Zeiss WL Research compound microscope
241 242 BULLETIN OF MARINE SCIENCE, VOL. 27, NO.2, 1977 equipped with phase and Nomarski differ- furnished by Dr. Marian H. Pettibone), come ential interference contrast optics. The from Texas (Port Aransas), Louisiana, Kodachrome slides were then projected on Florida (Panama City, Alligator Harbor, drawing paper with the aid of a Super Tampa Bay, Sarasota Bay, Broad River Chromega enlarger, and traced at the desired Delta in Everglades National Park, Seahorse scale, Drawings of entire larvae and juveniles Key), east coast of Florida (Marineland- were made free hand from living and pre- types of S. floridensis stephensoni Hartman, served specimens with the aid of compound 1949), Georgia (Sapelo Sound), South and dissecting microscopes, Carolina (Winyah Bay), and North Carolina Tubes of Phragmatopoma californica con- (Beaufort, Cape Hatteras). I have also col- taining several hundred sexually mature lected occasional specimens in shallow water specimens were purchased from Pacific Bio- on stones and shells offshore from Fort Pierce Marine Supply, Venice, California in July on the east coast of Florida, and on the spiny 1974. Adults were maintained in the labo- pen-shell, Atrina sp., scallop shells, and other ratory in aerated, fresh-filtered sea water pelecypods, which were washed ashore at (34%0) in a Percival E-30b environmental Sanibel Island, Lee County, and St. Peters- chamber at 17-18°C and fed every other burg Beach, Pinellas County on the west day with Dunaliella salina, Isochrysis gaibana, coast of Florida. and Chiorella autotrophica, The specimens Gamete-containing abdominal segments of were allowed to adjust to their new environ- mature males appear creamy-white, while ment for several days before spawnings were those of mature females are dark pink to lav- attempted. ender. Freshly spawned eggs range from Spawning and maintenance of eggs and 75-90 Jlm in diameter. Mature sperm possess larvae were carried out using the same pro- an elongate acrosome, thus modified from the cedures described above for Sabellaria flori- "primitive" polychaete type as defined by densis. Separate cultures of larvae were Franzen (1956). The head, including the maintained at two different temperatures: acrosome, is 6.4 Jlm in length while the tail 17-18°C and 21-23°C (room temperature). is about 32 J1.ffiin length. The early development parallels that of RESULTS other known sabellariids. The major differ- ences consist of a slightly slower rate of de- Larval Development of velopment in the early larval stages, the color Sabellaria floridensis of the larval chromatophores and the mor- Sabellaria fioridensis Hartman, 1944 phology of the opercular spines and paleac. Sabellaria fioridensis is a common inter- Ten to 12 h after fertilization, the trocho- tidal and shallow-shelf sabellariid polychaete, phares possess prototrochs, small apical tufts originally described from the west coast of and are swimming weakly. By 21 h, the Florida (Lemon Bay, Sarasota County) by apical tufts are larger, the posterior cilium has Hartman (1944). Additional published appeared and the larvae are swimming more records of this species include Playa de vigorously. The appearance of the first pair Tecolutla, Mexico (Rioja, 1946) and Alli- of provisional setae, four eyespots and ten- gator Harbor, Franklin County, Florida tacle buds all occur somewhat later than those (Hartman, 1951) in the Gulf of Mexico, of the two other sabellariids from Florida, and in North Carolina (Hartman, 1951; Sabellaria vulgaris and Phragmatopoma Day, 1973). Additional specimens of S. lapidosa, using the same culturing technique floridensis, on deposit in the United (see Table 1). States National Museum of the Smith- Older larvae (8-10 days) possess scattered sonian Institution, Washington, and checked yellow-green chromatophores which are by Dr. David Kirtley (information kindly gradually concentrated over the episphere. A ECKELBARGER: SABELLARIID LARVAL DEVELOPMENT 243
8
m o " 't: .. 3
c
A Figure 1. Larva of Sabel/aria floridensis A-C: A. dorsal view of late larval stage just prior to metamor- phosis (about 17 days old); B. primary palea from opercular peduncle; C, larval nuchal spines from different individuals. Abbreviations: c. opercular cirrus; dh, dorsal hump; e. eyespot; t. tentacle. distinct row of yellow-green chromatophores days), a single, narrow, greenish-brown pig- was observed in many larvae along the dorsal ment band forms over the dorsal and lateral and lateral posterior margins of the episphere, portions of the trunk segments. When the roughly outlining the prototroch. A similar tentacle buds appear (13-15 days), three of band of reddish-black chromatophores was these bands are present. found in Sabellaria vulgaris larvae (Eckel- Figure 1 shows a late larval stage about 17 barger, 1975). As development proceeds, days from fertilization. It agrees with previ- the chromatophores on the episphere develop ously described sabellariids, having four red brownish flecks which tend to mask the green eyespots, a pair of long tentacles, a well- color observed earlier. Bright green chro- developed prototroch and telotroch, two matophores appear on the pygidium and re- bundles of long, barbed, provisional setae, a main throughout larval development. Before dorsal hump posterior to the eye-spots, three the formation of tentacle buds (about 10-12 parathoracic segments with dorsal para- 244 BULLET]N OF MARINE SCIENCE, VOL. 27. NO.2, ]977
Figure 2. Larva of Sabel/aria floridensis in early stage of metamorphosis A-B: A, dorsal view; B, ventral view. Abbreviations: ab, first abdominal segment; bo, building organ; c, opercular cirrus; m, mouth; ne, neurotroch; no, nototroch; ns, nuchal spine; opp, opercular peduncle; pp. primary paleae; pt, first parathoracic segment.
podial lobes each bearing four capillary spines were observed in the larvae of S. setae and three abdominal segments with floridensis. Following metamorphosis, the dorsal uncinigerous lobes. nuchal spines will elongate and move closer The tentacles are about one-half the body to the midline near the eyespots. The black length and have yellow-green chroma to- dorsal pigment bands remain but may be phores scattered over their entire dorsal broken along the median line in some larvae. surfaces. This contrasts with the situation in The segmental bands extend ventrally, where P. lapidosa and S. vulgaris, in which the pig- they mayor may not meet the neurotroch. ment is concentrated in the distal portions of Metamorphosis and settlement occur 18- the tentacles. Yellow-green chromatophores 27 days afterfertilization, at 21-23°C. Meta- are dispersed in a ring over the episphere, the morphosis is similar to that found in other center being devoid of any pigmentation. The sabellariids. Figure 2 illustrates the begin- telotroch possesses lateral clusters of bright ning of metamorphosis with the loss of the yellow-green chromatophores and black pig- provisional setae and anterior rotation of the ment bands are present dorsally on the pos- larval tentacles, resulting in the exposure of terior borders of the parathoracic segments. the underlying opercular peduncles bearing Oil droplets are heavily concentrated in the the primary paleae, nuchal spines and oper- gut. Hidden among the provisional setae are cular cirri. The small nuchal spines have broad, spiny primary paleae (Fig. lB) and moved towards the midline away from the a pair of small nuchal spines (Fig. 1C), which paleae and nearer the eyespots. The epi- are the precursors of the adult nuchal spines. sphere is beginning to shrink and the heavily- Despite extensive observations, no opercular ciliated mouth region and building organ are ECKELBARGER: SABELLARlID LARVAL DEVELOPMENT 245
B Figure 3. Larva of Sahellaria floridensis in advanced stage of metamorphosis A-B: A, dorsal view; B, ventral view. Abbreviation: ns, nuchal spine.
beginning to differentiate. The prototroch is ent on the dorsal surface of the tentacles, still present ventrally. The pygidium termi- although not as many as earlier. Five bands nates in a conical extension bearing the anus of nototrochal cilia are present dorsally with and is reflexed slightly ventrally. The pri- two on the thoracic segments and three along mary paleae vary in number but seven or the posterior borders of the parathoracic seg- eight pairs are common. ments. The black pigment bands over the Figure 3 shows a larva in a more advanced dorsal surface of the body segments are begin- stage of metamorphosis with the tentacles ning to fade. The rudimentary parapodia of fully rotated and the paleae beginning to fol- the first thoracic segment are apparent as low. The episphere has been reduced to a short processes, anterior-lateral to the build- small median prostomial projection or cirrus, ing organ, and possess short sensory hairs or still bearing the eyespots and yellow-green bristles. Posterior and lateral to the building chromatophores. The dorsal hump remains organ are a pair of small projections repre- prominent but will soon disappear and the senting the rudimentary parapodia of the mouth region has undergone further differ- second thoracic segment. The three ab- entiation. dominal segments possess prominent uncini- Figure 4 shows a completely metamor- gerous lobes and the gut now contains only phosed larva which has taken up a sedentary existence after construction of a sandy tube. a few oil droplets. Ventral rami or neuro- The rotation of the peduncles and associated podia, each bearing two simple capillary paleae is complete and the medial prostomial setae, have developed on the three para- cirrus is now digitiform and heavily ciliated. thoracic and abdominal segments. The telo- Yellow-green chromatophores are still pres- troch is still present and the ventrally-flexed 246 BULLETIN OF MARINE SCIENCE, VOL. 27, NO.2, 1977
A
Figure 4. Fully metamorphosed larva of Sabellaria floridensis A-B: A, dorsal view; B, ventral view. Abbreviations: ns, nuchal spine; rp, rudimentary parapodia of first and second thoracic segments; vp, ventral parapodial ramus of first abdominal segment.
telotrochal swelling bears the anus on its inner rows, have appeared (Fig. 5D,E). The conical tip. larval nuchal spines have been replaced by Figure 5 shows a juvenile worm about 3 two larger pairs just lateral to the eycspots weeks after metamorphosis and settlement. (Fig. 5A,F). The opercular cirri have en- The yellow-brown pigment, which previously larged and a second pair has formed. The covered the long tentacles, has now disap- median prostomial cirrus has become more peared except for some pigment which may slender and still bears the eyespots. The remain at the tentacle tips in some specimens. anterior-most region of the mouth, just poste- The opercular peduncles have differentiated rior to this structure, bears flecks of dark into more adult-like structures. The primary pigment. Similar pigmented areas are also paleae have been lost and replaced by the first found along the lateral lips of the mouth. A type of outer paleae (Fig. 5C). Additional sixth and seventh row of dorsal nototrochs paleae, possibly representing the middle and have appeared on the first and second abdom- ECKELBARGER: SABELLARllD LARVAL DEVELOPMENT 247
A B Figure 5. Juvenile of Sabel/aria floridensis about 3 weeks after metamorphosis A-F: A, dorsal view; B, ventral view; C, outer opercular palea; D, E, opercular paleae, probably representing middle and inner rows; F, nuchal spine. Abbreviations: ca, caudal appendage; ft, feeding tentacle; ns, nuchal spines. inal segments and the uncinigerous noto- and abdominal segments. The telotroch has podiallobes of the abdominal segments have been lost and the conical structure bearing elongated. The black pigmented bands have the anus has elongated into a caudal appen- almost disappeared dorsally, but still persist dage, which is reflexed ventrally. The yellow- laterally and ventrally on some segments. brown pigment is still present on the caudal Black pigment spots have developed around swelling representing the last vestiges of the the ventral neuropodia of the parathoracic telotrochal swelling. 248 BULLETIN OF MARINE SCIENCE, VOL. 27, NO.2, 1977
Larval Behavior.- The behavior of Sabellaria recently, Roy (1974) discussed their tube- floridensis larvae in the laboratory differed dwelling behavior. significantly from the larvae of S. vulgaris, The larval development of Phragmatopoma Phragmatopoma lapidosa and P. californica, californica is so similar to that recently cultured under nearly identical conditions. described for P. lapidosa (Eckelbarger, 1976) The larvae of S. floridensis demonstrated no that a detailed description is considered un- definite reaction to light during the entire necessary. Aside from their larger size and developmental period, unlike larvae of the overall brighter pigmentation, the larvae of above-mentioned species which remained P. cali/ornica are virtually impossible to dis- photopositive until near the end of develop- tinguish from those of P. lapidosa. The two ment. S. floridensis larvae swam randomly species are certainly closely related; the over the bottom of the culture jar when cir- adults are very similar and the egg and sperm culation was removed, rather than aggregat- are virtually identical in size and morphology. ing nearest the light. The gamete-containing abdominal seg- Another strikingly different behavioral pat- ments of mature males appear creamy-white, tern, not previously reported in sabellariids, while those of mature females are dark was observed in Sabellaria floridensis larvae. greenish-grey in color. In the present study, In the absence of tube-building materials, egg diameter ranged from about 80-105 p'm, such as sand grains and detritus, more with 90-100 p.m being most common. How- than half of the larvae metamorphosed nor- ever, Hartman (1944) reported the eggs of mally in some of the cultures. After tube- P. californica to be about 70 p'm in diameter, building material was added a day after meta- while Dales (1952) reported 75 p'm as the morphosis, the larvae crawled over the bot- average size. The significance of these dif- toms of the culture bowls for several days, ferences is unknown. exploring the substrate before finally building Mature sperm possess a pointed, curved tubes. Initially, larvae constructed only acrosome, thus modified from the "primitive" mucous tubes, adding sand to them from a type as defined by Franzen (1956). The few hours to a few days later. Some larvae sperm head, including the acrosome, is about constructed sandy tubes and remained in 6 p'min length, while the tail is about 36 p.m. them, while crawling about the cultures on A timetable of development for Phragma- their tentacles, dragging their tubes with topoma californica is included in Table 1. them. The only noticeable differences between the larvae of P. californica and P. lapidosa is the Larval Development of overall larger size of P. californica larvae at Phragmatopoma californica equivalent stages in development and their Phragmatopoma californica (Fewkes) brighter pigmentation. Both species possess yellow-green chromatophores over the epi- Phragmatopoma californica (Fewkes) is a sphere and telotrochal regions but those of reef-building sabellariid ranging intertidally P. lapidosa are duller. to about 80 m, from California south to The primary paleae and opercular spines Ensenada, Mexico and Lower California of both species are very similar; examination (Hartman, 1944). A few general comments of large numbers of larvae failed to reveal any on development were presented by Hartman consistent differences. The size and mor- (1944) and a partial description of larval phology of the primary opercular paleae vary development was published by Dales (1952), widely within a single specimen and repre- in connection with his study on the develop- sentative figures for P. lapidosa (Fig. 6G-I) ment of the anterior region. Scholl (1958) and P. californica (Fig. 6J-L) have been reported the effects of their tube-building included to illustrate this variation. activities on the sorting of beach sand. More The growth rate of Phragmatopoma cali- ECKELBARGER: SABELLARIID LARVAL DEVELOPMENT 249 fornica larvae differed substantially at the two different culturing temperatures, with meta- morphosis and settlement occurring between 18 and 25 days from fertilization at 21-23°C and between 34 and 39 days at 17-18°C, or nearly 60% longer at the colder temperature. I Settled larvae in culture from the colder I i,'I' I 1\~ water were maintained in the laboratory for 8 "~1 '1;;1: months. During this period, the juveniles ,\I' constructed a large aggregation of tubes over ~i_ ,;/,I" the bottom of the gallon culture jar and reached a maximum body length of about 18 mm. The worms were adult-like in every feature, including the opercular paleae, al- though no sex products were observed. An experiment was undertaken to deter- mine how long adults of P. californica could survive when removed from their tubes and maintained in culture dishes in filtered sea water at 21-23°C (room temperature) and 17-18°C. Specimens were fed the same diet as the larvae and their water was changed weekly for a total period of 3 months. Speci- mens maintained at room temperature died at the end of 2 months but those kept at 17-18°C remained healthy and active until the experiment was terminated.
Comparison of Primary Opercular Paleae, Figure 6. Primary opercular paleae from sabel- lariid larvae A-L: A, Sabel/aria floridensis; B, Opercular Spines and Nuchal Spines in Sabellaria vulgaris (from Eckelbarger, 1975); C, Larvae of Sabellariidae Sabel/aria spinulosa (from Wilson, 1929); D, Although sabellariid larvae of most species Sabel/aria alveolata (from Wilson, 1929); E, Lygdamis indicus (from Bhaud, 1975b); F, Lyg- studied to date are morphologically similar in dal11is muratus (from Bhaud, 1975a); G-I, Ph rag- their early larval stages, the appearance of matopoma lapidosa (from Eckelbarger, 1976); J-L, different kinds of opercular spines and paleae Phragl11atopoma californica. in their later larval stages provide a con- venient means for separating genera and often species. overlapping of forms. Since the adults of Figures 6 and 7 show the morphology of these two species appear to be closely related, the primary opercular paleae and spines, the similarities in their larval structures are respectively, of sabellariid larvae, based in not surprising. However, since the published part on literature sources. Of the primary geographical ranges of the two species do not paleae and opercular spines shown in these overlap, it seems unlikely that their larvae figures, only those of Phragmatopoma would be encountered together in the plank- lapidosa and P. californica are so similar as to ton at any single locality. be almost impossible to differentiate. The The primary opercular paleae (Fig. 6) paleae represented (Fig. 6G-I and J-L) are probably offer the greatest opportunity for variations commonly encountered within a the study of generic relationships, because single individual and clearly demonstrate an they are larger and more numerous and there- 250 BULLETIN OF MARINE SCIENCE, VOL. 27, NO.2, 1977
other hand, are transitory or rudimentary structures which arise along the bases of the provisional setae in each opercular peduncle in the late larval stages and disappear after settlement and metamorphosis. Opercular spines have been described from all species of sabellariids studied, with the exception of Sabellaria floridensis larvae, which seem to lack them. The nature of the opercular spines is unclear. With the exception of Lygdamis spp., they do not superficially resemble any chitinous structure in the adult operculum. A B The nuchal spines (Figs. IC, 3A, 4A) c appear in the larvae at about the same time as the opercular spines, on the inner side of the opercular peduncle below the level of the paleae and just lateral to the eyespots. Larval opercular spines have been recorded for S. floridensis (Figs. Ie, 3A, 4A), S. vulgaris and S. alveolata. The adults of all but the latter species also possess opercular nuchal spines. The larval nuchal spines are similar in morphology and position to those of the adult (Fig. SA) and probably are homol- ogous. A key to the pelagic larvae of the Florida sabellariids, Phragmatopoma lapidosa, Sabel- D E F G laria vulgaris and S. floridensis, is presented, based on the pattern of tentacle pigmentation Figure 7. Larval opercular spines or "crown and the morphology of the opercular spines bristles" from sabellariid larvae A-G: A, Sabel/aria vulgaris (from Eckelbarger, 1975); B, Sabel/aria and paleae. spinulosa (from Wilson, 1929); C, Sabel/aria alve- u/ata (from Wilson, 1929); D, Lygdamis indicus KEY TO THE PELAGIC SABELLARIID (from Bhaud, 1975b); E, Lygdamis muratus (from LARVAE OF FLORIDA Bhaud, 1975a); F, Phragmatopoma lapidosa (from Eckelbarger, 1976); G, Phragmatopoma cali- 1a. Larval tentacles with scattered yellow- lamica. green chromatophores and reddish-black or dark brown pigment flecks over distal half of dorsal surface (may be concen- trated into more definite spots distally) 2 fore easier to identify than are the opercular 1b. Larval tentacles with yellow-green chro- spines. The primary paleae of three species, matophores over entire dorsal surface; without pigment flecks (Fig. IA). Bright Sabellaria floridensis, S. vulgaris and S. green chromatophores on pygidium. Pri- spinulosa (Fig. 6A-C), superficially resemble mary opercular paleae spatulate, with the outer opercular paleae of the juvenile and heavy marginal spines and straight, pro- longed tips (Fig. 6A). Opercular spines adult worms and are probably homologous. absent. Nuchal spines pointed and usually However, little resemblance is observed curved at tip with minute denticIes distally (Figs. IC, 3A) Sabel/aria Iloridensis between the larval primary paleae and the 2a. Primary opercular paleae broad, oar-like, adult outer opercular paleae in the other with tips usually curved and pointed, with sabellariids studied. small denticIes along one margin (Fig. 6G-I). Opercular spines single type, with The opercular spines (Fig. 7), on the straight shaft bearing 4 or 5 rings of blunt ECKELBARGER: SABELLARIfD LARVAL DEVELOPMENT 251
teeth distally (Fig. 7F). Nuchal spines barger (1976) found that the larvae of no~ present Phragrnatoporna lapidosa 2b. Pnmary opercular paleae similar to S. Phragmatopoma lapidosa were rather un- floridcnsis but with narrower blade and selective in their choice of sand. The precise smooth p~oximal portion longer and nar- selectivity in S. alveolata and S. spinulosa, rower (FIg. 6B). Opercular spines of 2 types, each with slightly swollen distal por- however, might represent a mechanism for tions bea~ing fine denticles (Fig. 7A); reproductive isolation, since they are com- nuchal spmes curved, with fine denticles mon sympatric species in the Plymouth area. along one edge distally Sabellaria vulgaris S. alveolata forms massive reefs on intertidal Table 1 includes a summary of larval de- rocks, while S. spinulosa builds sandy tubes velopmental times based in part on literature on the surface of stones and shells on the sources. The developmental stages were bottom of the Sound and elsewhere below selected because they are relatively easy to low-water mark (Wilson, 1929). Differences recognize, making them useful for com- in larval substrate specificity might result in parison. a general spatial separation of the two popula- tions. P. lapidosa, the only reef-building DISCUSSION sabellariid in Florida waters, shows little sub- strate selectivity, which may reflect the ab- The early works of Mortensen (1921) on sense of spatial competition from other echinoderm larvae and Wilson (1932) on sabellariid species. S. vulgaris, a Florida east Mitraria polychaete larvae, demonstrated for coast species sympatric with P. lapidosa, the first time that substrate played an im- comm?nly constructs solitary or small ag- portant role in the ability of invertebrate gregatIOns of tubes on shells and rocks in the larvae to metamorphose. The studies by subtidal areas of the shelf, and also encrusts Wilson (1968a, b, 1970a, b) on substrate rocks intertidally along jetties, although not specificity in the sabellariids, Sabellaria in direct competition with P. lapidosa. While alveolata and S. spinulosa, demonstrated that the latter species builds tubes on the outer deprivation of a suitable substrate could pre- vent or delay larval metamorphosis for ex- surfaces of the rocks where they are directly exposed to strong wave action and tidal cur- tended periods in these polychaetes. That is not universally the case in polychaetes, how- rents, S. vulgaris prefers the more protected caves and inner surfaces of the jetties. S. ever, for Simon (1968) demonstrated that floridensis is not as common on the east th.e larvae of Spio setosa metamorphosed coast of Florida and therefore is probably not without substrate of any kind. Thorson in competition with either species. (1966), while acknowledging that some The ability of Sabellaria floridensis larvae species have very specific substrate prefer- to metamorphose in the absence of a sub- ences, suggested that most species are prob- strate in the laboratory is a feature of sabe1- ably not highly discriminatory at the time of lariid behavior unreported until now. The metamorphosis or become less so the longer wide variety of substrates upon which the a substrate is absent. Reporting on a 3-year worms build their tubes also suggests that this study of the Oresund, Muus (1966) pre- species does not share the strong depth and sented data suggesting that many polychaete larvae settle on substrates unsuited to later substrate specificity of the primarily rock- existence and in the course of a few weeks adherent species, such as S. alveolata, Phrag- disappear entirely from the benthos. matopoma lapidosa and P. californica. It is apparent that substrate specificity Hurley (1973), studying the settlement among sabellariids also varies. While Wilson behavior of the subtidal acorn barnacle , clearly demonstrated the precise selectivity of Balanus pacificus, a species which settles on Sabellaria alveolata and S. spinulosa larvae small ephemeral objects in the sand rather for the tube cement of their own species, the than the more populated rocky intertidal latter species being the most selective, Eckel- communities, concluded that the cypris larvae 252 BULLETIN OF MARINE SCIENCE. VOL. 27, NO.2, 1977
.•.o .g
<') <') 00 <') N N- N c-. c-. c-. c-. I c-. c-. I I I -- (""'0- -N N_ N- ..c o ..c:: ..c:: N N I -I o o 00 o <') N - -N N ..c:: ..c ..c ..c ~ N N ..c ..c N I I I I -N -o -o N N -o - 00 - - - - - V> '0" Q, tn" ECKELBARGER: SABELLARIID LARVAL DEVELOPMENT 253 lacked a strong preference for substrate and function of this structure has not been investi- depth, thus permitting the exploitation of a gated. large variety of substrates as they become An examination of Table 1 demonstrates available. A parallel situation may exist with the range of settlement times that have been S. floridensis. reported for different species of sabellariids. The prolonged crawling behavior demon- With the exception of Sabellaria alveolata strated by Sabel/aria floridensis larvae is also and S. spinulosa, the settlement times of the a unique behavioral pattern among the sabel- species listed are remarkably similar, ranging lariids. Furthermore, as far as I am aware, from 2 to 8 weeks. However, the extremely no other tube-building polychaete studied to long development times for S. alveolata and date, possesses such a post-metamorphic S. spinulosa (from 6 to 32 weeks for the exploratory period. Wilson (1929), in his former species, according to Wilson, 1970a), detailed study on the post-metamorphic be- are probably not representative of the true havior in S. alveolata, noted that larvae who development times of either species in na- failed to construct mucous tubes initially after ture. Wilson ( 1929) suggested that 6 weeks, metamorphosis, were unable to build sandy the earliest settlement time recorded in his tubes later. Wilson (1968a) also noted that experiments, most likely represented the time construction of a tube is usually accomplished taken at sea. Thorson (1946) also suggested quickly after metamorphosis. My observa- that the shortest periods of pelagic develop- tions on S. vulgaris, P. lapidosa and P. cali- ment in laboratory studies probably corre- fornica agree with those of Wilson, that fol- spond most closely to the natural conditions. lowing metamorphosis tube-building was If this assumption is made in the case of rapid. The unusual delay in tube-building Wilson's work, then a developmental period by S. floridensis in the laboratory suggests of 6 weeks for S. alveolata and S. spinulosa that a brief period of migration and explora- is not as different from that of other sabel- tion precedes final settlement in the field. lariids as it may first appear. Indeed, Wilson Since this species is commonly encountered (1970a) reported that S. spinulosa larvae on widely-scattered small solid substrates, taken in the plankton completed development such as sand dollar tests, decapod carapaces, in the laboratory in 5.5 to 12 weeks. How- pelecypod shells, stones and surf grass, this ever, he estimated duration of larval life in period would allow larvae to explore wide the plankton to be nearer 6 to 8 weeks. areas of the shelf and locate relatively small Mauro (1975) recently suggested that the objects upon which to construct tubes. premetamorphic development rate of the Of particular interest during S. floridensis tropical species, Phragmatopoma lapidosa, larval development is the dramatic reduction was considerably faster than those of the in size of the head region (episphere) during temperate species, S. alveolata and S. spinu- metamorphosis, ultimately resulting in the losa, based on laboratory studies. The latter two species, however, based on their reported formation of a median, ciliated prostomial distribution along the eastern north Atlantic, projection, called the "median cirrus" by Day southern North Sea, English Channel, the (1967: 671). Wilson (1929: 235) similarly Mediterranean and northwest Africa (Hart- described a "ciliated conical process" in the mann-Schroeder, 1971), are considered to be larvae of S. alveolata and S. spinulosa. The warm-temperate, being present in the north- function of this structure, which enlarges and ern extremes of warm-temperate biogeo- persists in the adult, is unknown. It is present graphical provinces as defined by Hedgpeth in all species of Sabellaria whose develop- (1957) and Briggs (1974). Briggs (1974) ment has been studied and was figured by stated that the relatively warm water of the Bhaud (1975a: 162, fig. 3A) in the larva of North Atlantic Current made it possible for Lygdamis muratus. As far as I am aware, the a warm-temperate fauna to exist as far north 254 BULLETJN OF MARINE SCIENCE, VOL. 27, NO.2, 1977 as the English Channel and that even during stirred than in unstirred dishes and usually the coldest month of the year, the sea surface sooner, with more larvae settling in stirred temperature of southern England is about dishes with sand, than without. the same as that of North Carolina just north It is apparent that the settlement times of of Cape Hatteras. Crisp and Southward sabellariid larvae may vary when the cultur- ( 1958) and Stephenson and Stephenson ing techniques differ with regard to the (1972) reported a northward extension of a degree of culture agitation, the presence or large number of warm-water species, includ- absence of sand, the size of the culture ves- ing S. alveolata, into the southern and south- sels, the temperature, light, food, and general western regions of the British Isles. Labo- laboratory procedures. Therefore, caution ratory developmental studies on the tropical must be taken in making comparisons be- species, P. lapidosa (Eckelbarger, 1976), tween larval development times of different and the three warm-temperate species, S. species, based on laboratory evidence. vulgaris (Eckelbarger, 1975), S. floridensis and P. californica (present study), show no ACKNOWLEDGMENTS significant differences in development time The author wishes to tbank Mrs. P. A. Linley when using the same temperature and cul- for her excellent assistance in the maintenance of turing technique. the larval cultures. Special appreciation is ex- Thorson (1946, 1950) discussed the pressed to Dr. Marian H. Pettibone of the Na- effects of temperature on larval development tional Museum of Natural History, Smithsonian and stated that development of larvae living Institution, for reviewing the manuscript and pro- viding many helpful suggestions and constructive in seas of higher temperatures appear to be criticisms. This work represents contribution num- generally the same as those inhabiting ber 54 from tbe Harbor Branch Foundation, Inc. northern seas. Within a given area, however, temperature has a significant influence on the LITERA TURE CITED duration of larval life. Bhaud, M. 1969. Developpement larvaire de The role of temperature on sabellariid de- Phalacrostemma cidariophilum Marenzeller, velopment has been demonstrated in the lab- 1895. Vie et milieu, SeI. A, BioI. 20: 543-557. oratory. The settlement time of Sabellaria --. 1975a. Nouvelles donnees sur les larves vulgaris larvae increased from 19 to 35 days de Sabellariidae recoItees en MeditelTanee. after a decrease in temperature from 23 Ann. Ins!. Oceanogr. 51: 155-172. D --. 1975b. Nouvelles observations de Sabel- to 19 C (Curtis, 1973). The larval develop- lariidae (Ann elides Polycbetes) dans la region ment time of Phragmatopoma californica was Malgacbe. Cah. O.R.S.T.O.M., Ser. Oceanogr. increased from 18 to 25 days to 34 to 39 days 13: 69-77. resulting from a decrease in temperature from Briggs, J. C. 1974. Marine Zoogeography. Mc- Graw Hill, Inc., New York. 475 pp. 21 to 23 DCto 16 to 18DCrespectively (pres- Cazaux, C. 1964. Developpement larva ire de ent study). Sabel/aria alveolafa (Linne). Bull. Ins!. In a previous paper (Eckelbarger, 1975), Oceanogr. Monaco 62: 1-]5. it was reported that the development times Crisp, D. J., and A. 1. Southward. 1958. The from fertilization to metamorphosis in Sabel- distribution of intertidal organisms along the coast of the English Channel. J. Mar. BioI. laria vulgaris and Phragmatopoma lapidosa Ass. U.K. 37: 157-208. were reduced up to 50% when the cultures Curtis, L. 1973. Aspects of the life cycle of were agitated through vigorous aeration. Wil- Sabellaria vulgaris Verrill (Polycbaeta: Sabel- son (1970b ) reported an increase in the lariidae) in Delaware Bay. 236 pp., Ph.D. thesis, University of Delaware. rate of S. spinulosa settlement with the inser- Dales, R. P. 1952. The development and struc- tion of a bubbling air tube into the culture. ture of the anterior region of the body in the In addition, Wilson (1968a) reported that in Sabellariidae, with special reference to Phragmatopoma califomica. Q. J. Microsc. most instances metamorphosis (settlement) Sci. 93: 435-452. of S. alveolata larvae occurred earlier in Day, J. H. 1967. A Monograph on the Poly- ECKELBARGER: SABELLARIID LARVAL DEVELOPMENT 255 chaeta of Southern Africa. Part 2. Sedentaria. Marine Biological Laboratory, Woods Hole, The British Museum (Natural History), Lon- Mass. Lancaster Press, Lancaster, Penn. don Publication number 656: 459-878. Rioja, E. 1946. Estudios anelidol6gicos. XIV. 1973. New Polychaeta from Beaufort, Observaciones sobre algunos poliquetos de las with a key to all species recorded from North costas del Golfo de Mexico. An. Jnst. BioI. Carolina. NOAA Tech. Rep. NMFS SSR-F (Univ. Nac. Anton) Mexico. 17: 193-204. Circ. No. 375. 140 pp. Roy, P. A. 1974. Tube dwelling behavior in the Eckel barger, K. J. 1975. Developmental studies marine annelid Phragmatopoma californica of the post-settling stages of Sabellaria vulgaris (Fewkes) (Polychaeta: Sabellariidae). Bull. (Polychaeta: Sabellariidae). Mar. BioI. 30: So. Calif. Acad. Sci. 73: 117-125. 137-.149. Scholl, D. W. 1958. Effects of an arenaceous .1976. Larval development and popula- tu be-building polychaete upon the sorting of tion aspects of the reef-building polychaete a beach sand at Abalone Cove, California. Phragmatopoma lapidosa from the east coast Compass 35: 276-283. of Florida. Bull. Mar. Sci. 26: 117-132. Simon, J. L. 1968. Occurrence of pelagic larvae Franzen, A. 1956. On spermiogenesis, mor- in Spio setosa Verrill, 1873 (Polychaeta, phology of the spermatozoan and the biology Spionidae) Bio!' Bull. 134: 503-515. of fertilization among invertebrates. Zool. Stephenson, T. A., and A. Stephenson. 1972. Bidr. Upps. 31: 355-482. Life between tidemarks on rocky shores. W. Hartmann-Schroeder, G. 1971. Annelida, Bors- H. Freeman and Co., San Francisco. 425 pp. tenwlirmer, Polychaeta. In, Die TierweIt Thorson, G. 1946. Reproduction and larval de- Deutschlands, Jena 58: 1-594. velopment of Danish marine bottom inverte- Hartman, O. 1944. Polychaetous Annelids. Part brates, with special reference to the planktonic VI. Paraonidae, Magelonidae, Longosomidae, larvae in the Sound (0resund). Meddr. Ctenodrillidae, and Sabellariidae. Alan Han- Kommn. Danm. Fish. -og Havunders. (Ser. cock Pacif. Exped. 10: 311-389. Plankton) 4: 1-529. 1949. A new marine annelid from 1950. Reproductive and larval ecology Florida. Proc. U.S. Nat. Mus. 99(3250): of marine bottom invertebrates. BioI. Rev. 503-508. 25: 1-45. 1951. The littoral marine annelids of 1966. Some factors influencing the re- the Gulf of Mexico. Pub\. Jnst. Mar. Sci., cmitment and establishment of marine benthic Univ. Tex. 2: 7-124. Hedgpeth, J. W. 1957. Marine biogeography. communities. Neth. J. Sea. Res. 3: 267-293. Pages 359-382 in J. W. Hedgpeth, ed. Treatise Wilson, D. P. 1929. The larvae of the British on marine ecology and paleoecology. Geo!. sabellarians. J. Mar. BioI. Ass. U.K. 16: 221- Soc. Am. Mem. 67. 269. Hurley, A. C. 1973. Larval settling behavior of 1932. On the Mitraria larva of Owenia the acorn barnacle (Balalllls pacificus Pilsbry), fllsiformis Delle Chiaje. Phil. Trans. London, and its relation to distribution. J. Anim. ser. b, 221: 231-334. Eco!' 42: 599-609. 1968a. Some aspects of the develop- Mauro, N. A. 1975. The premetamorphic devel- ment of eggs and larvae of Sahel/aria alveolata opmental rate of Phragmatopoma lapidosa (L.). J. Mar. BioI. Ass. U.K. 48: 367-386. Kinberg, 1867, compared with that in tem- 1968b. The settlement behavior of the perate sabellariids (Polychaeta: Sabellariidae). larvae of Sabellaria alveolata (L.). J. Mar. Bull. Mar. Sci. 25: 387-392. BioI. Ass. U.K. 48: 387-435. Mortensen, Th. 1921. Studies of the develop- 1970a. Additional observations on lar- ment and larval forms of echinoderms. 266 val growth and settlement of Sabellaria aille- pp. K~benhavn: G.E.C. Gad. olata. J. Mar. BioI. Ass. U.K. 50: 1-31. Muus, K. 1966. A quantitative 3-year survey on 1970b. The larvae of Sabellaria spin- the meiofauna of known macrofauna com- IIlosa and their settlement behavior. 1. Mar. munities in the Oresund. Veroff. lnst. BioI. Ass. U.K. 50: 33-52. Meeresf. Bremerhaven, Sonderbind 2: 289- 292. DATE ACCEPTED: April 14, 1976. Novikoff, A. B. 1957. Pages 93-97 in D. P. Costello et a\., eds. Methods for Obtaining ADDRESS: Harbor Branch Foundation, Inc., RFD and Handling Marine Eggs and Embryos. 1, Box 196, Fort Pierce, Florida 33450.