Early Larval Development of Polydora nuchalis Woodwick, a Spionid Polychaete

KEITH H . WO ODWICK1

THE MOST RECENT detailed work treating the are a synth esis of a series of observations of in­ larval development of Polydora, that of Han­ dividuals from a number of egg cases. The ages nerz (1 956 ) , app eared a little more than one assigned "the various stages are not absolute but, century after Oersted ( 1843) described for the because they are based on multiple observations, first time a larval stage in Polydora ciliata are considered to be reasonable. (Johnston ), Wilson 1928."Related papers pre­ sented during the interval includ ed those of COMPOSITE POLYDORA LIFE HISTORY Claparede ( 1863), Agassiz (1867), Jacobi An und erstanding of the larval development ( 1883 ), Whitelegge ( 1890 ), Andrews ( 1891 ) , of polydorids is expedited by an understanding Mesnil (1896) , Leschke (1 90 3) , Soderstrom of the relationship of these larval stages to the ( 1920 ) , Wilson ( 1928 ), Rioja ( 1939 and remainder of the life history. A comp osite life 1941) , Hart man (1 94 1), Thorson (1946 and history of memb ers of the genus is presented 1950 ) , Smidt (1952 ), and C asanova (1952 ) . below; P. nuchalis follows this scheme in most Each of these added information valuable to the stages but does show individual differences. und erstanding of polydorid development , but, as yet, in only a few forms is the early develop­ A composite life history as extracted from ment known in detail. the literature may be summarized in the fol­ Th e purpose of this paper is to make known lowing manner. An adult male and female copu­ the early developmental stages of a recently de­ late. Fertilization is internal. Th e female spawns scribed polydorid, Polydora nuchalis W oodwick the fertilized eggs through the nephridial canal (1953) . and into transparent "capsules. The capsules, formed in the manner described by Soderstrom METHOD (1920) , are attached to the inn er wall of the female's tub e or burrow. Cleavage of the fer­ The developmental stages of P. nuchalis were tilized egg is complete but unequal. Further de­ cultured either in petri dishes containing sea velopment of larvae within the egg capsule water and sand from the original collecting area follows one of two types: ( 1) In Polydora or in aquaria of circulating aerated sea water ciliata (W ilson, 1928 ) and certain other species after the method of Reish (1953 ). Favorable re­ sults were obtained with both of these methods. each egg in the capsule gives rise to a larva. The Observations were made of encased larvae (in larvae leave the capsule at the 3-segment (seti­ egg capsules) as well as free-swimming indi­ gerous segment ) stage as planktotrophic forms viduals. Th e study of living material on depres­ to begin a long planktonic period ( four to six sion slides provided specimens unaltered by weeks) pri or to settl ing and metamorph osis. fixation or cover glass pressure. Drawings of ( 2) In Polydora boplza« (W ilson, 1928) which living forms were made empl oying the tech­ represents the other type, each egg in the cap­ nique of Wilson (1928) and were inked fol­ sule does not give rise to a larva. Th e few which lowing a comparative study of several other do develop, feed on the undev eloped eggs larvae of the same age group. " (nurse eggs). The larvae begin feeding at about The drawings do not constitute a continuous the 3-segment stage but do not leave the capsule developmental series from one individual but until about the 12-segment stage. The hatched larvae pass through a very short planktoni c 1 Department of Biology, Fresno State College, stage, if any, before settling and metamorphosis. Fresno, Californ ia. Manuscript received October 13, 1958. The latter type of developm ent is found in

122 Polydora nuchalis- W OODWICK 123

P. nuchalis. Larvae leave the egg capsules after Early Larva, 36 H ours. ( Plate I, Fig. 4.) The having fed on nurse eggs until the 9- to 12­ anreroventral prolongation is no longer present segment stage ( Plate I, Fig. 1). Further studies , in this stage and the larva measures only 120 !J­ to be reported in another paper, suggest that in length. The anterior part of the larva remains male and female do. not copulate as such; a transparent ; the posterior part is filled with yolk reciprocal transfer of sperm involving two pro­ granules. The prototroch, not apparent in this randric males occurs. Th e stored sperm fertilize figure, is limited mainly to the ventra l region. the eggs which develop in the later female stage The formation of the vestibule and the anterior of prorandry in each individual. Protandry and portion of the gut has been initiated. also neoteny have been reported for Polydora Late Presegm ent Larva, 72 H ours. ( Plate I, hermaphroditica Hannerz ( 1956) . Fig. 5.) The larva has elongated and does not Polydora nuchalis does, however, follow rather so closely resemble the egg as did the two pre­ closely the composite life history in the remain­ ceding larval stages. Th e larva is about 200 !J­ ing developm ent . The larval stages described long, nearly doubl e the length of the pr eceding below are not unlike those figured for other stage; however, it has no true segments as yet. species of Polydora. The anterior and the posterior body regions are transparent with the yolk pr esent in the central EARLY DEVELOPMENTAL STAGES OF region serving as an excellent ind icator of the Polydora nuchalis intestina l porti on of the digestive traer. Th e transparency of the posterior region is a result Egg. ( Plate I, Fig. 2.) The eggs are round of the development of the pygidium. The telo­ and about 120 !J- in diameter. Th ey include a troch is well developed and prominent. The central mass of light pink yolk granules and a prototroch is present laterally, just p osterior to very narrow peripheral region which is tran s­ the two eyes. The lateral eyes are the first pig­ parent. The yolk granules described here appear ment areas to be formed. Differentiation of the in the gut of all the developing stages up to at head and body has begun . least 10 segments and are useful in determining Early T suo-Segment Larva, Five Days. This the developm ental boundaries of the gut in all larva, 0.26 mm. long, has two complete segments these stages. and the beginning of a third pair of setal sacs. Cleavage of the egg is total but unequal as Two pairs of eyes are now present in the trans­ has been reported for other polydorids. parent anterior region. The palpi are beginning Early Larva, 18 Hours . ( Plate I, Fig. 3.) Th e to bud laterally just posterior to the eyes. Th e . larva, 180 !J- long, is transparent anteriorly, the developm ent of the vestibule has continued; the yolk granules being concentra ted in the pos­ mouth proper is visible. Th e posterior gut has terior half. The primordia of the perisromium begun to invaginate but has not joined the and prostornium are set off by ridges. This stage central concentration of yolk granules. The has an unusual anteroventral prol ongation of pygidium is set off from the rest of the body the larval body. The prol ongation was noted by a depression in the body surface which con­ in more than one series of larvae but no sug­ tains the base of the cilia of the relotroch. The ' gestion can be made here as to its significance. first pair of dorsal melanoph ores is located on It may be abnormal, but its repeated appearance the primordia of the third segment. and the fact that larvae of this kind continued T hree-Segm ent Larva, Six Days. (Plate II, to develop in a normal fashion later have led to Fig. 1.) The larva, 0.30 mm . long, has thr ee its inclusion to allow comparison with possible well-developed segments. It is tran sparent ex­ future investigations on this and other species. cept for segments two and three in which the The prototroch is located on the ventrolateral gut contai ns yolk granules. surface near the juncti on of the main body of The palpi have thickened but have not elon­ the larva and the anterovenrral prolongation. gated. The prorroch and telotroch are as de­ The telotroch has appeared also but is lacking scribed for the prev ious stage. The pygidium from a wide dorsal porti on. is cone-shaped and papillated;·its appeara nce is 124 PACIFIC SCIENCE, Vol. XIV, April 1960

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PLATE 1. Fig. 1. Egg capsules and larvae. Fig. 2. Egg, 0.12 mm .Fig. 3. Early larva (18 hours), 0.18 mm . Fig. 4. Earlylarva (36 hours), 0.12 mm . Fig. 5. Late p re-setiger larva (72 hours), 0.20 mm . Polydora nuchalis- WOODWICK 125

similar to that described by Hartman (1941 ) eleventh segment nearly complete in its develop­ for an unknown spionid larva. The melano­ ment. The larva illustrated does not contain phores on the third segment have elongated nurse egg material although it is often found in laterally and another pair has formed on the de­ . the gut of larvae of this and later stages. The veloping fourth segment. large ventral vestibule passes food into the long, This 3-segment stage has thr ee pairs of eyes. ciliated esophagus from which it moves to the Later, the two pairs which are antero lateral fuse intestine beginning at segment four. The anus on each side producing a single anterolateral opens in the central portion of the pygidium pair. Four eyes, the fused pair and the median which has become flattened. The dorsal notch pair, are retained throughout life. characteristic of the adult pygidium is not The vestibule has enlarged but has not as present. yet opened to the granular intestinal portion of The eyes are as in the previous stage, but the gut. The ciliated posterior invagination of the palpi are more elongate. N otopodial lobes the gut nearly reaches the third segment and are present in all the segments. Those of the after a few additional hours of development its first segment are located more dorsally than the cavity becomes joined to that of the granular others and are, thus, nearer the midline. The intestinal portion. This junction, along with neuropodial lobes of the first segment are on completion of the vestibular porti on, will pro­ the same lateral plane as the noropodial lobes duce a functional digestive tract. In larvae hav­ of the other segments. This condition prevails in ing a long pelagic life, completion of the gut the adult. Branchiae are not present. Melano­ development and hatching are concurrent and phores are present on segments three and four larvae are able to feed upon leaving the egg as paired dorsal elongations and on the succeed­ cases; this is usually at the 3-segment stage. ing six segments as paired dots which dim­ Polydora nuchalis does not hatch at the 3­ inish in size on the more posterior segments. segment stage but does begin to feed on the Segments two, seven, and eight have lateral nurse eggs. The stage at which gut development pigment spots. The pygidial melanophore is is completed, however, is not so critical in a present. A single stout spine is situated in the species of Polydora having nurse eggs. notop odium on each side of the modified fifth Five-Segment Larva, One Week. This larva segment. is about 0.50 mm. in length. It has five setiger­ Fift een-Segmen t Larva, T hree Weeks. (Plate ous segments and at least three more segments III. ) This form repr esents the settling stage of which are forming. The entire animal is trans­ P. nuchalis. It is similar in appearance to the parent except for a few yolk granules present adult, but will be discussed here as the final in the gut. Most larvae of this size have a larval stage. It is 0.90 mm. in length and has 15 complete digestive tract includ ing a vestibule, fully developed segments and a sixteenth partly esophagus, intestine, rectum, and anus. The developed. vestibule, esophagus, and rectum are greatly Th e anterior end is adultlike with the peri ­ ciliated. stomium and prostomium greatly developed in The palpi have elongated but the prototroch, comparison with previously described stages. telotroch, and pygidium are as described for the The prostornium is bilobed anteriorly. Two pairs preceding stage. Two pairs of eyes are present of eyes are located on the prostomium. The in the normal adult position with the lateral nuchal tentacle, one of the diagnostic characters pair anterior to the median pair. for P. nuchalis, is now present on the posterior The dorsal paired melanophores are elon­ part of the prostomium. Th e elongate palpi gated on segment three and smaller pairs are which arise from the peristomium extend as far present on segments four and five. There is also as the modified fifth segment. Each of the palpi a single pygidial melanophore. has a median ciliated groove used in the feeding T en -Segment Larva, About T wo lY/eeks. process. The central body portion, like the an­ (Plate II, Fig. 2.) This larva is 0.65 mm. in terior portion, resembles that of the adult but length and has 10 segments formed with the the pygidial portion does not. The pygidium is 126 PACIFIC SCIENCE, Vol. XIV, April 1%0

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PLATE II. Fig. 1. 3-seciger larva (six days) , 0.30 m m. Fig. 2. lO-seciger larva .(cwo weeks), 0.65 mm. Polydora nuchalis- WOODWICK 127 broad and flangelike but certain changes in ciliary tracts and pigmentation associated with metamorphos is; to be mentioned below, have yet to occur. The vestibule leads into a long esophagus which joins the intestine at the anterior end of the sixth segment and a long rectum extends from about segment ten to the posterior end of the body. Cilia are pr esent in the vestibule, esophagus, and rectum but are not indicated in the figur e. The prototroch and telotroch are ordinarily lost shortl y after settling occurs as one of the changes in the metamorphosis from larva to adult. Gastrotrochs, not menti oned pr eviously, are found on segments three, five, seven, ten, thirteen, and fifteen. Th ese ventral, ciliary tracts first appear on segment thr ee in early stages of development and on succeeding segments (o f the numbers mentioned above) as development continues. Th ey are importa nt locomotor organs in the short free-swimming period of P. nuchalis and the longer free-swimming periods of forms which hatch at the 3-segment stage. The conspicuous dorsal melanophores are present only on segments twelve and thirteen and will be lost from these in succeeding stages. The pygidial melanophore and lateral pigment spots present on segment eight and the right side of segment nin e are lost in metamorphosis. While in the egg capsule and until shortly after hatching, the larvae are positively pho totropic; but at the time of settling and metamorphosis the melanophores and pigment spots are lost and the larvae become negatively phototropic. This suggests rather strongly a functional relation­ ship between the phototropic change and loss of pigmentation. Two heavy spines are present in each noro­ podium of the modified fifth segment, the larg­ est of the body segments. Neuropodi al hooded hooks appear first in segment seven. Branchiae also appear first on segment seven and in the 15-segment stage are partly formed on segment eight, as well. The larvae ordinarily hatch at the 12-segment stage, but they may leave the egg case at the 9-segment stage. The larvae settle, metamor-

P LATE III . I5 -setiger larva (three weeks), 0.90 mm . 128 PACIFIC SCIENCE, Vol. XIV, April 1960

phose, and build tubes duri ng the 13- to 17­ terne chez les Annelides, Les Spionidiens des segment stage. cotes de la Manche. Bull. Sci. Fr. Belg. 29: The adult characteristics are considered in 110-287. Woodwick (1953 ). OERSTED, A. S. 1843. An nulatorum danicorum conspectus, Fasc. 1. Maricolae. Pp. 1-52. ACKNOWLEDGMENTS REISH, D . J. 1953. Description of a new tech­ T he writer is indebted to the Biology D epart ­ nique for rearing polychaetous annelids to ment of the Un iversity of Southern Californ ia sexual maturity. Science 118 ( 3065): 363­ and to th e Allan H ancock Foundation for re­ 364. search space and equipment and to . Dr. Olga RIOJA, E. 1939. Estudios anelidologicos I. Ob­ H artman, Dr. John 1. Mohr, and D r. D onald ]. servaciones acerca de varias formas larvarias Reish for invaluable assistance. y postlarvarias pelagicas de Spionidae, prece­ dentes de Acapulco, con descripcion de una especie nueva del gen era Polydora. Ann. Inst, REFERENCES BioI. Univ. Mex. 10: 297- 311. AGASSIZ, A. 1867. On the young stages of a few --- 1941. Estudios anel idologicos III. Datos annelids. An n. Mag. N at. H ist. Ser. 3, 19: para el conocimiento de la fauna de Polique­ 203-218, 242-257. tos de las costas del Pacifico de Mexico. Ann . ANDREWS, E. A. 1891. A commensal annelid. Inst. BioI. Univ. Mex, 12: 669-746. Amer. Nat. 25: 25-35. SMIDT, E. 1. B. 1952. Animal production in CASANOVA, 1. 1952. Sur Ie developpement de the Danish W adde nsea. Medd. Komm. H av­ Polydora antennata ( Claparede ). Arch. Zool. unders¢g . Kb h. 11 (6) : 1-151. Exp. Gen. 89 ( 3) : 95-101. SODERSTROM, A. 1920. Studien tiber die Poly­ CLAPAREDEj.:E 1863. Beobachtungen tiber Ana­ chaetenfamilie Spionidae. D issertation. Upp­ rornie und Ent wicklungsgeschichte wirbel­ sala. (Almquis t and W icksells.) 286 pp. loser Thiere an der Kiisre von Normandie THORSON, G. 1946. Reproduction and larval anges rellt. vii + 120 pp. Leipzig. development of Danish marine bottom in ­ H ANNERZ, 1. 1956. Larval development of the vertebrates, with special reference to the polychaete families Spionidae Sars, Disomidae planktonic larvae in the Sound ( 0 resund) . Mesnil, and Poecilochaetidae n. fam. in the Medd. Komm. H avunders¢g. Kbh. 4 ( 1) : Gu llmar Fjord ( Sweden) . Zool. Bidr . Upp­ 1-523. sala. 31: 1- 204. --- 1950. Reproductive and larval ecology H ARTMAN, O. 1941. Some contributions to the of marine bottom invertebrates. Biol, Rev. biology and life history of Spionidae from 25: 1-45. Californ ia. Allan H ancock Pacif. Exped. 7: WHITELEGGE, T. 1890. Report on the worm 289-324. disease affecting the oysters on the coast of JACOBI, R. 1883. Anatomisch-histo logische Un­ N ew South Wales. Rec. Aust. Mu s. 1: 41-53. tersuchung der Polydoren der K ieler Bucht. WILSON, D .P. 1928. The larvae of Polydora In augural D issertation. Kiel . (\'\7eissenfels, ciliata John ston and Polydora hoplura Clap­ Leopold Kell ) . 37 pp. arede. J. Mar. BioI. Ass . UK 15: 567-603. LESCHKE, M. 1903. .Beirrage zur Kennt nis WOODWICK, K. H. 1953. Polydora nuchalis, a der pelagischen Polychaetenlarven der Kieler new species of polychaetous annelid from Fohrde, Wiss. Meeresuntersuch. 7: 113-134. California. ]. Wash. Acad . Sci. 43(11) : 381­ MESNIL, F. 1896. Etudes de morphologie ex- 383.