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On the History of grubei (Kinberg), a from Californial

PAUL C. SCHROEDER2

RELATIVELY LITTLE INFORMATION is yet avail­ of February the are more abundant in able on the life histories of nereid holdfasts of the highest specimens of the brown from the eastern Pacific. Johnson (1943) has kelp Egregia menziesii. In order to collect the raised some intriguing problems concerning animals from their in the kelp the N ereis vexillosa, which have not been further holdfasts must be removed from the rock with explored, and Smith (1950) has reported de­ a hammer and chisel and carefully dismembered. tails of the life history of Nereis limnicola During the summer only a few, usually very (= lighti) , an interesting viviparous, small specimens can be recovered from these euryhaline . Information is also available holdfasts; this was tested by allowing summer­ for a southern Californian population of N el'eis collected holdfasts to stagnate in a pan until grubei, a species which reproduces more typi­ animals emerged from the inaccessible inter­ cally. The present paper deals with a central stices. It seems probable that the move Californian population of N. grubei from Pes­ into the kelp holdfasts for the winter, when the cadero Point, Monterey County. Interesting dif­ surf is most violent. Such seasonal habitat shifts ferences between these .two populations with are known in other intertidal animals from this respect to physiology and breeding season have area as well (e.g., the isopod Idothea monterey­ come to light during the course of an investiga­ ensis [see Lee, 1966]). tion of nereid (Schroeder, The habitat reported by Reish (1954b) for 1967) . the species at Point Fermin in southern Califor­ nia appears to be somewhat different. He found HABITAT N. grubei in algal tufts in or between tidepools scoured from a wide, flat rock ledge. The ledge At Pescadero Point, Monterey County, Cali­ is strewn with scattered boulders and sheltered fornia, N ereis grubei occurs on an exposed from the surf by offshore kelp beds. At Point coast where the surf can be quite violent, even Fermin the was found to be associated though offshore kelp beds are well developed. with a number of different species of algae, The intertidal region is composed chiefly of chief among which is Cladophora trichotoma. large boulders covered with abundant algae of This alga occurs in central California as well, many species. The worms may be found here in and a search through tufts of it near the Hop­ two different situations, in which their abun­ kins Marine Station, not far from Pescadero dance varies with the season. During the spring Point, failed to yield any specimens of N. grubei, and summer they are most readily found in the although the worm occurs beneath Gastroclo­ sandy substrate beneath the common red alga nittm in the same area. Although Reish surveyed Gastroclonium cottlteri. Some specimens may be the algal associates of the species at Point Fer­ found in this situation throughout the year, but min he mentions neither Egregia menziesii nor from the beginning of October until the middle Gastroclonium cottlteri, the two major algal as­ sociates at Pescadero Point. The former is not 1 A portion of a dissertation submitted to the Graduate Division of Stanford University in partial found south of Point Conception, but the latter fulfillment of the requirements for the degree of is recorded from as far south as San Diego Doctor of Philosophy. Manuscript received Septem­ (Smith, 1944). It thus appears that the more ber 26, 1967. northerly population favors Gastroclonium, de­ 2 Hopkins Marine Station, Pacific Grove, California. Present address: Department of , Washington spite the presence of Cladophora, and that the State University, Pullman, Washington 99163. opposite is true for the southern population 476 Life History of Nereis grubei-ScHROEDER 477

(although I do not know whether Gastroclo­ and sought, but not found.) Such nearly ma­ nium is abundant at Point Fermin). ture animals probably swarmed within a couple In an ecological study at the Hopkins Marine of days of being observed, although swarming Station, not far from Pescadero Point, small itself was never observed. numbers of N. grubei were found by Glynn The fact that maturing animals are found on (1965) in association with another alga, En­ separate occasions, and not in intervening pe­ docladia muricata. This alga is not included in riods, implies that specimens within the popula­ the list given by Reish for the southern Califor­ tion mature at different times. It should thus be nia population. possible, in midwinter population samples, to separate animals destined for different spring­ time spawnings. OOGENESIS AND METAMORPHOSIS Oocytes have been shown to grow at two dif­ N ereis grubei was collected every two weeks ferent rates, both in N. grubei (Schroeder, at Pescadero Point, Monterey, California, for a 1966) and in N. diversicolor (Clark and Rus­ period of 17 months. During the period of ton, 1963). Thus in N. grubei the oocyte oogenesis the average oocyte diameter was de­ growth rate (rate of diameter increase) seems termined for a number of specimens from each to accelerate when the oocytes are about 100"" collection; the number of specimens so deter­ in diameter, and it is at about this time that the mined varied with experimental requirements. first histological signs of metamorphosis can be All diameters were measured from fresh coelomic detected (Schroeder, 1967). This fact is utilized samples with a calibrated ocular micrometer and in Figure 1 in an attempt to follow the develop­ a compound microscope. Fixation in Bouin's ment of each monthly swarm within the popu­ fluid made up with picric-acid-saturated sea lation as a whole. The dotted lines are projec­ water was found to cause an irregular expansion tions based upon the apparent time of swarming, of the oocytes (Schroeder, 1966). In some ani­ estimates of the growth rate during the two mals, oocytes of considerably different diameters phases, and the recorded oocyte diameters. It is were present, but in most of these the recorded assumed that the oocyte growth rates are similar diameters fell into distinct size classes. In such in the component animals of successive spawn­ cases only the average diameter of the largest ings. Each month on the graph has been sub­ size was utilized in the life history study. divided into 3-day periods, so that the positions In the few cases in which size classes were not of the points within a month are significant to evident, the diameters of all the oocytes from a within three days. It will be seen that during single were averaged together. It is the fall animals with oocytes of a wide range of probable that such figures are lower than the sizes are present, but that these are not separ­ value truly comparable to the others. The aver­ able into distinct groups until December, when age oocyte diameter was used as an index to most specimens can be assigned to a spawning the age of female animals. group, even though the oocytes are still small Oocytes could be found in at least a few ani­ and growing slowly. It is possible that the dif­ mals throughout the year. Oogonia and tiny ferent spawning groups are distinct from the oocytes appear in June, when very few matur­ initial moment of oogonial differentiation, but ing females remain from the previous year's the variability of oocyte sizes present in young spawning group. The oocytes probably reach animals prevents their recognition. maturity (about 200",,) in 7-8 months. The A number of animals was maintained in the young oocytes grow slowly through the fall and laboratory over a period of weeks and the growth early winter, and the population gives rise to of their oocytes was checked by repeated samp­ several swarms between mid-February and mid­ ling. These sampling points have also been in­ June. The occasions on which nearly mature cluded in Figure 1 and are connected with females were found in the field are indicated by heavy lines. It will be seen that all but two of the short vertical bars at the top of Figure 1. these animals were derived from the April (The 0 in mid-March represents a day on spawning group, while two others metamor­ which metamorphosing animals were expected phosed sooner and were closer to the March

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i,SO / /. ,.: 11' 1/ ,:/ // // 130 / A:' . I J .M ',, ~ 110 ...-r:' J/ tj!-//J/i ~ o {~-:':>l:::lJ;>/ "!'j g90 . / ...... (') /xl~,> /l /'; /' en 70 ::~;-2tJj~~:~:::l' (') 50 II ! <: 30 r ii' 'j , .. i / i , ,::: ," i"· ii' .1 , ~ I~'; Jan; Feb Mar Apr May June July Aug SepfOcf Nov Dec Jan Feb Mar Apr MayJune July Aug ~~ f ~ 1965 MONTHS 1966 B ~...... ilf FIG. 1. Oocyte development and swarming in Nereis grubei at Pescadero Point, Monterey County, California. Each point in the 1966 series represents the average oocyte diameter of an animal collected on the date indicated. Dotted lines represent the postulated progress of several subgroups within the population o,.., toward their respective swarming dates. Solid lines represent growth rates from individual animals. The solid line on the left connects the largest oocyte S- diameters found in each collection. Days on which very mature specimens were found ,in the field are indicated by a vertical line through the delimited zone O"' ~ which includes the range of oocyte diameters found in swarming females. The zero represents a day on which no such animals were found; the dotted line ..... in this group (in May) is an estimated swarming date based on laboratory observations. Vertical stippled lines indicate the time of the full moon through \0 0\ the collecting period. The 1965 collections were incomplete due to inadequate knowledge of the habitat of the species. 00 Life History of Nereis gmbei-ScHROEDER 479 group. It is felt that these data provide concrete from which at least a few animals swarmed evidence in support of the projected swarming monthly until June. groups. One of the swarms (represented in Figure 1 A line has also been drawn connecting the by the heavy dotted line over May 1966) has largest oocytes found in each collection before been inferred from the fact that two animals the first swarm in February. The oldest animals taken from the field on April 26 swarmed si­ in each of these collections ought to be those multaneously in the laboratory on May 19. A destined to participate in the first swarm and search of the Gastroclonium on May 22 failed should therefore represent a single swarming to reveal any metamorphosing animals; this is group. This line was used to estimate roughly what would be expected if the animals in the the growth rate of the oocytes during each phase laboratory had swarmed simultaneously with a and to localize the size range during which the group in the field. growth rate increases. The line suggests an The dates of the full moon for several months oocyte growth rate of about 1.8f!/day during the of breeding activity during the winter of 1965­ second, rapid phase. Oocyte growth rates were 1966 have been indicated by vertical dotted also determined for 14 animals with oocytes bands in Figure 1, since nereid breeding ac­ over 100f! in diameter maintained in the lab­ tivity has often been correlated with the phase boratory, as mentioned above. These indicated a of the moon (Korringa, 1947; Hauenschild, growth rate of 1.74±0.49f!/day. This growth 1966). It should be recalled that the observa­ rate estimate is also supported by data from a tion of metamorphosing animals in the field single unfed animal which was brought into the must antedate the swarming of these same ani­ laboratory with ll1-f! oocytes. It swarmed 62 mals, so that the swarming dates indicated in days later. Assuming a final oOGyte diameter of Figure 1 are -all somewhat early.- Furthermore, 200f!, the oocytes in this individual must have the theory of Hauenschild (1966) suggests grown at a rate of about 1.4f!/day. The average that the moon phase might correlate at the point growth rate, during the final period of rapid where the oocyte growth rate increases rather growth, is thus between 1.6 and 1.7f!/day. The than at the time of actual swarming. It is not growth rate may not be constant throughout the known whether a latent period occurs between period of rapid growth in N. grubei, and a defi­ the supposed lunar stimulus and the observed nite slowing down of growth as the maximum response; the figures presented, do not, in my size is approached has been reported for N. opinion, either affirm or deny a possible phase­ diversicolor (Clark and Ruston, 1963). setting relationship with the lunar cycle. The The first swarming takes place in February, fact that subgroups are separable within the and evidence has been found for a swarm each population in early December suggests that month until June. Each swarm seems to involve some determination of the spawning groups has fewer animals than the one preceding it, so that occurred before the time that the oocyte growth the bulk of the population swarms in February rate has increased within any group. This adds a and March. In February virtually all the ma­ third point in time for the possible intervention turing animals in the Egl'egia holdfast habitat of environmental stimuli in determining the disappear; subsequent swarms arise from the breeding periodicity (see discussion by Clark, Gastroc!onium. This fact accounts for the lack 1965). of data for the spring of 1965. Collections were made during this period, but only from the COMPARISON WITH A SOUTHERN CALIFORNIAN holdfasts, which were almost totally devoid of POPULATION maturing animals. After the discovery of N. grubei beneath Gastroc!onium, both habitats At the outset of this work a definite breeding were monitored during the spring of 1966. season had not been expected, since Reish Again mature animals disappeared suddenly and (1954b) reported that the population at Point almost completely from the Egregia holdfasts Fermin showed continual reproduction through­ during February. However, a significant popu­ out the year, and that specimens in some stage lation remained beneath the Gastroc!onium of metamorphosis could be taken at any time. 480 PACIFIC SCIENCE, Vol. XXII, October 1968

The two populations thus differ in the very oogenesis alone lasts 7 to 8 months, and much presence of a breeding season in the population smaller animals than those in which gametes are at Pescadero Point. found may be collected simultaneously. The de­ Constant breeding can be considered as an velopment time at Pescadero Point is therefore extremely prolonged breeding season. The aver­ 2 to 4 times as long as the laboratory develop­ age ocean temperature at Point Fermin is several ment time for specimens from the Point Fermin degrees higher than at Pescadero Point, and a population. lengthening of the breeding season in the south­ Whether these differences are simply expres­ ern portion of the range of temperate zone sions of latitudinal variation within a species, is known in other groups, e.g., the or whether they indicate that a deeper distinc­ Arbacia punctulata (Harvey, 1956). tion exists between these two populations can­ Additional examples are discussed by Giese not be determined from the available informa­ (1959) and Clark (1965). tion. The morphological identity of the two Other differences have been noted between forms has been graciously confirmed by Dr. the two populations. The heaviest female re­ Reish, who has clarified the taxonomic position ported by Reish weighed approximately 50 mg, of the species in conjunction with his work on and smaller specimens seemed to be the rule, its life history (Reish, 1954a). at least in his laboratory-raised animals. The largest female found at Pescadero Point weighed SUMMARY more than 1 gram, and mature females usually weighed in excess of 500 mg; the animals in the 1. The major algal associates of Nereis grubei Pescadero Point population are thus an order of at Pescadero Point, Monterey County, Califor­ magnitude heavier than those in the Point Fer­ nia, are Egregia menziesii and Gastroclonium min population. coulteri. The Egregia holdfasts contain more an­ A further difference between the populations imals during the fall and winter. involves the site of origin of the oocytes. Reish 2. At Pescadero Point, Nereis grubei breeds (1954b) found them to originate from a solid from February to June in approximately monthly tissue within the parapodia, from which clumps swarms. of oocytes are released upon achieving a diameter of up to 20Il. Such a parapodial tissue has never 3. Animals collected in December may be as­ been observed in N. grubei from Monterey signed to a specific swarming group by deter­ County, although oogonial proliferation has mining each animal's average oocyte diameter. been demonstrated autoradiographically in small clumps of oogonia floating free in the 4. The average rate of oocyte growth between (Schroeder, 1966). Mature oocytes from ani­ 1O01l and 200l! is 1.6-1.7IIIday. This repre­ mals in the Point Fermin population were found sents more rapid growth than is shown by smaller oocytes. to range in diameter from 1621l to 380Il. At Pescadero the size range was much narrower, 5. The central Californian population differs 1901l to 2lOIl. Oocytes within a given mature from that in southern California in its limited female are very uniform in size. breeding season, in the average size of the com­ Reish (1954b) raised specimens from the ponent individuals, and in the internal site of Point Fermin population to maturity in his lab­ oogenesis. oratory and found that while they usually meta­ morphosed after 28 to 29 weeks, exceptional ACKNOWLEDGMENTS specimens metamorphosed at as early as 14 weeks of age. This variability recalls that ob­ The author warmly appreciates the assistance served by Hauenschild (1966) in of Dr. Isabella Abbott in identifying the algae, dumerilii. Although the life span of a worm of Mrs. Dana Pierce in preparing the figure, of from the Pescadero Point population is not Dr. Donald Reish in definitively identifying the known, it must be close to a year at a minimum, worms, of Dr. Donald Abbott in critically re­ and is more likely to be 2 years. The period of viewing the manuscript, and especially of Dr. Life History of Nereis grubei-ScHROEDER 481

Arthur Giese, under whose patient guidance KORRINGA, P. 1947. Relations between the this work was carried out. It was supported by moon and periodicity in the breeding of U. S. Public Health Service Fellowship GM marine animals. Ecol. Monogr. 17(3) :347­ 17,007. 381. LEE, WELTON L. 1966. Color change and the REFERENCES ecology of the marine isopod Idothea (Penti­ dothea) montereyensis Maloney, 1933. Ecol­ CLARK, ROBERT B. 1965. Endocrinology and the ogy 47(6) :930-941. reproductive of polychaetes. Ocean­ REISH, DONALD J. 1954a. Nomenclatural ogr. Mar. BioI. Ann. Rev. 3:211-255. changes and redescription of two nereids CLARK, ROBERT B., and R. J. G. RUSTON. 1963. from the Eastern Pacific. Bull. So. Calif. The influence of extirpation on oogen­ Acad. Sci. 53, pt. 2:99-106. esis in the polychaete N ereis diversicolor. Gen. Compo Endocrinol. 3(5) :529-542. --- 1954b. The life history and ecology of the polychaetous annelid Nereis grubei (Kin­ GIESE, ARTHUR C. 1959. Comparative physiol­ ogy: annual reproductive cycles of marine berg). Occas. Pap. Allan Hancock Founda­ invertebrates. Ann. Rev. Physio1.21:547-576. tion 14:1-75. GLYNN, PETER W. 1965. Community composi­ SCHROEDER, PAUL C. 1966. A Histological and tion, structure and interrelationships in the Autoradiographic Study of Normal and In­ marine intertidal Endocladia muricata - Bal­ duced Metamorphosis in the Nereid Poly­ glandula association in Monterery Bay, chaete Nereis grubei (Kinberg). Disserta­ California. Beaufortia 12 :1-198. tion, Stanford University. 170 pp. HARVEY, ETHEL B. 1956. The. American Ar­ --- 1967. of epitokous bacia and Other Sea Urchins. Princeton Uni­ setae during normal and induced metamor­ versity Press, Princeton, N.J. 298 pp. phosis in the polychaete annelid Nereis HAUENSCHILD, CARL. 1966. Der hormonale grubei (Kinberg). BioI. Bull. 133(2) :426­ Einfluss des Gehirns auf die sexuelle Ent­ 437. wicklung bei dem Polychaeten Platynereis SMITH, GILBERT M. 1944. Marine Algae of the dumerillii. Gen. Compo Endocrinol. 6(1) :26­ Monterey Peninsula. Stanford University 73. Press, Stanford, Calif. 622 pp. JOHNSON, MARTIN W. 1943. Studies on the life SMITH, RALPH I. 1950. history of the marine annelid N ereis vexil­ in the viviparous polychaete Neanthes lighti. losa. BioI. Bull. 84(1) :106-114. J. Morph. 87(3):417-466.