Pacific Science (1983), vol. 37, no. 2 © 1983 by the University of Hawaii Press. All rights reserved

Morphological Variability during Longitudinal Fission of the Intertidal , Anthopleura elegantissima (Brandt)!

KENNETH P. SEBENS 2

ABSTRACT: The sea anemone Anthopfeura elegantissima forms clonal aggre­ gations on rocky shores along the Pacific Coast ofNorth America by a process of longitudinal fission. Fission can occur by lateral stretching of the column and separation of the two halves followed by internal regeneration of parts of the actinopharynx and of the column. Two new directive mesenteries, one sipho­ noglyph, and several pairs of mesenteries flanking the directives also form . Alternatively, large individuals appear to form new directive mesenteries and siphonoglyphs well in advance of division.

THE MOST COMPLETELY DESCRIBED cases of of food. Both use specialized organs longitudinal fission and clone formation in for agonistic behavior against other anem­ sea anemones are those of Halipfanella luciae ones and other clones of the same species (Verrill) and Anthopfeura elegantissima [acrorhagi in Anthopfeura (see Francis 1973b, (Brandt) . Halipfanella luciae divides rapidly 1976), catch-tentacles in Halipfanella (see and continuously when fed (Minasian 1976, Williams 1975)]. Anthopfeura elegantissima is 1979, 1982; Minasian and Mariscal 1979; dioecious and reproduces sexually each year Shick and Lamb 1977), forming dispersed (Sebens 1981b), but it is less clear that H. clones covering large areas of intertidal rock luciae reproduces sexually regularly, if at all (Uchida 1932, 1936; Kiener 1971 ; Williams (Shick 1976). 1973, 1975; Shick 1976; Shick and Lamb The ecological and physiological aspects of 1977)on shores around much ofthe northern longitudinal fissionare better understood than and southern hemispheres. Its rate of division are the morphological rearrangements neces­ and size at division are strongly temperature sary to effect division. Several studies have dependent (Miyawaki 1952, Johnson and described the fission of Halipfanella luciae Shick 1977,Minasian 1979)as are those of A. (Davis 1919; Atoda 1954, 1976), which tears elegantissima (see Sebens 1980). itself in two and subsequently regenerates the Anthopfeura elegantissima divides once or missing parts. Such rearrangement and re­ less per year (Sebens 1979, 1980, 1982a) and generation have also been described for forms dense aggregated clones (Hand 1955; anemones that reproduce asexually by other Francis 1973a, 1979; Fredericks 1976; Sebens methods including pedal laceration (Torrey 1977, 1981a,b, 1982b, in press) in the intertidal and Mery 1904, Hammat 1906, Cary 1911 , zone of rocky shores along the west coast of Stephenson 1929) and transverse fission North America. Unlike Halipfanella luciae, (Schmidt 1970). The present study is the first fission isinhibited when A . elegantissima is fed description of the morphology oflongitudinal (Sebens 1980). Fission thus occurs primarily fission in Anthopfeura elegantissima and during the fall, winter, and early spring when points out the apparent occurrence of two the anemones are capturing the least amount distinct mechanisms of fission.

1 Manuscript accepted 4 February 1983. METHODS 2 University of Washington , Department of Zoology, Seattle, Washington 98195. Present address: Harvard Serial sections of individuals at various University, Museum of Comparative Zoology, Cam­ stages of division were prepared to investigate bridge, Massachusetts 02138. the morphological reorganization that must 121 122 PACIFIC SCIENCE, Volume 37, April 1983 occur in order to effect longitudinal fission in RESULTS Anthopleura elegantissima. Anemones were collected (during 1973-1977 and 1982) at The pedal disc is normally approximately Tatoosh Island (48°24' N, 129°48' W), Iceberg circular. It is not uncommon, however, to Point (48°25' N, 122°53' W) on Lopez Island, observe individuals with the longest dimen­ and Cattle Point (48°27' N, 122°5TW) on San sion of the pedal disc several times that of the Juan Island, Washington. Specimens appear­ shortest. This posture is assumed when an ing to be in some stage of fission were im­ individual conforms to a very thin crack in mediately pinned to slabs of paraffin in as a rock surface, or when squeezing between close to the natural posture as possible with obstacles in its path . It also occurs when the the pedal disc against the paraffin. If not so anemone is in motion, the axis of elongation restrained , the tension between the two halves being the same as the direction oflocomotion, caused them to curl so that the oral surface in which case the pedal disc is not very far became very concave, indicating that tension from circular. Elongation is often followed was greater along this surface than along the by a return to the circular pedal disc. Such pedal disc. Pinned anemones were relaxed in a elongated postures, which superficially re­ I : I mixture of 7.5 percent MgCI2 and sea semble the first stage of longitudinal fission water at 5°C for 24hr, then fixed in Bouin's (Figures 1, 2B), differ in the shape of the oral solution. aperture, which is rounded or slightly oval in Specimens were embedded in paraffin or, if an individual not undergoing fission. In anem­ very large, in Parlodion (seemethod in Sebens ones commencing fission, the two ends of 1981 b). Sections of Parlodion-embedded the pedal disc are actively moving apart and specimens, 25 and 50.um thick, were collected may show a partial inflation of the edges as in groups of five and stained, with each group is common during locomotion. The adhesive in a separate jar so that a serial array was verrucae of the column are arranged in closely maintained. Sections were stained with Hei­ packed vertical rows at opposite ends of the denhain 's Azan or Azan modified for Par­ column along the long axis and are spread lodion. A total of 63 anemones was fixed and wide apart along the short axis (Figure 2D) . embedded, 42 of which were used in this The latter area is stretched by the movement study. Six additional specimens were dis­ of the two ends of the pedal disc. The entire sected after relaxation, and many more were oral disc is elongated, and the tentacles are observed and photographed alive in the field more sparse in the area under tension. The at all stages of division. siphonoglyphs lie at the two extreme ends of Two hundred anemones , collected at Cattle the actinopharynx along the long axis at the Point in June and July 1974,were dissected to beginning of the elongation. Later, if the de­ determine the incidence in the population of velopment of a second set of siphonoglyphs siphonoglyph numerical abnormalities. Two occurs, the original ones may be shifted some­ siphonoglyphs each supported by a pair of what away from the ends of the long axis. directive mesenteries (diglyphy) is the most Division of the column commences aborally common arrangement, but monoglyphic and and continues in an oral direction followed triglyphic individuals do occur. Several immediately by closure of the column wall dividing anemones in the sectioned material where separation occurs. The initial elonga­ had four siphonoglyphs and four sets of direc­ tion progresses as the pedal disc divides into tive mesenteries (tetraglyphy), which could two separate portions which continue to move occur if a second pair had formed just prior to apart. The anemone is now free of the sub­ or during division. Alternatively , tetraglyphic stratum underneath the central portion, al­ states may represent division of a normally though the entire body is often pulled flat tetraglyphic polyp. The second case might against the substratum. At this point a probe be expected if some percentage of the non­ can be passed underneath the center of the dividing population were found to be tetra­ dividing anemone without dislodging either glyphic. of the two pedal disc halves. Finally, the two Morphological Variability during Fission of the Sea Anemone-SEBENS 123

FIGURE I. An elongated individual of Anthopleura elegantissima in the process oflongitudinal fission. The anemone has probably already divided the actinopharynx and is still attached by the oral disc and the column. Limekiln Lighthouse Point , San Juan Island, Washington, July 1982(scale bar = 0.5em).

halves are held together only by the oral disc tentacles in the region above the strip of light­ and by the marginal sphincter muscle. The colored tissue. Eventually, the actinopharynx actinopharynx can be seen through the open is completed and the two siphonoglyphs are oral aperture as having divided although still positioned at opposite ends of the actino­ connected along its oral rim. Separation of pharynx as new mesenteries and body-wall the actinopharynx and oral disc occurs next, tissue are added. If the division results in and the two halves are then connected only monoglyphic halves, a new siphonoglyph by the marginal sphincter (Figure 2F), which arises from the scarred area in each daughter appears as two thin bands of tissue stretched individual. between the halves. These bands eventually The timespan of division is highly variable . give way, one at a time, resulting in complete In newly collected anemones, longitudinal fis­ separation. sion has been completed in as short a time as The broken ends of the upper column and 5 days. In other individuals the process has sphincter then roll inward and fuse, com­ proceeded over 6 to 8 wk. The first stage of pleting the formation of two separate indi­ elongation lasts the longest, with the actual viduals (Figure 2H). At this stage, a strip of separation occurring in a period ofa few days smooth light-colored tissue is visible running or less. The new individuals produced retain vertically from the pedal disc to the parapet the light-colored strip of tissue for at least where closure of the column wall has been 1mo and as long as several months (Sebens effected. The actinopharynx is not yet com­ 1980, 1982a), although the pharynx is com­ plete orally and has two free edges facing the plete and centralized approximately 1 to 2 wk axis of division. There is a conspicuous lack of after division. At the early stages the column

.:..:...... :...;..•._..~- ~ '. B

o

o s--I-Nf!

F IGURE 2.Longitudinal fission ofAnthopleura elegantissima (originally diglyph ic type). A, C, E, and G are internal views; B, D , F, and H are external. A, B: A diglyphic nondividing individual or one just prior to division. Note the circular oral aperture. Sipho noglyph (8), longitudin al retractor muscle (M) ofdirective mesentery (D), actino phary nx (A), basal extension of direct ive mesentery (B). C, D :Beginning ofdivision. Elongation of the oral aperture, basal notch (N) formation in the actinop hary nx and widening of complete mesenter ial endocoels (E) perpendi cular to axis of division. No te that the pedal disc in D is partially inflated in the direction ofmovement of each half and that the vertical rows of verrucae are separa ted where division willocc ur. E, F: Late division stage. The act inoph arynx division is almost complete, and the two daughter actinopharynxes have not yet fused at their basal ends (F).The individual in F is slightly furth er along toward separat ion than that in E. The body wall has divided and the two new individuals are held together only by the marginal sphincter and upper body wall. The ora l disc is held close to the substratum but has been raised in this diagram to show the lower column. G, H : Postdivision daughter individuals. When the sepa ration has been effected, the upper port ion of the actinopharynx has.yet to fuse. New directive (N D) mesenter ies and other mesentery pairs will form opposite the old . Note the white division scars in H . Morphological Variability during Fission of the Sea Anemone-SEBENS 125

TABLEI

SIPHONOGLYPH A RRANGEMENT IN A POPULATION A nthop/eura e/egantissima C OMPARED TO T HAT IN D IVIDING AND RECENTLY DIVIDED INDIVIDUALS

FIELD POPULATION DIVIDERS POSTDIVISION

SIPHONOGLYPH DIAMETER DIAMETER ARRANGEMENT N (em ± s.d.) N (em ± s.d.) N

M o noglyphie 5 1.0 ± 0.1 0 0 6 Dig lyphie 187 1.4 ± 0.5 19 1.2 ± 0.5 3 Trigl yphie 8 1.7 ± 0.3 0 0 0 Tetraglyp hie 0 0 6 1.5 ± 0.6 0

T otal 200 1.4 ± 0.5 25 1.3 ± 0.5 9

NOTE Diameter of divider s is the average of longest and nar rowest diameter; that of po stdivider s was not taken.

is very elongated horizontally as is the oral separation of the whole anemone. Rather, aperture. Ho wever, internal reorganization final division of the actinopharynx is just has hardly begun at this point. For this reason, prior to that of the oral disc, immediately pre­ many of the specimens sectioned show little ceding separation of the collar and marginal more than the beginnings of actinopharyngeal sphincter. Fusion of the oral margin of the division and widening of the spaces between actinopharynx occurs some time after sepa­ mesenteries perpendicular to the axis of elon­ ration of the two halves of the anemone. gation. In fact, several of the anemones col- . Of the 25 anemones showing division to lected either were in the very early stages of the stage of actinopharynx division, 6 were longitudinal fission or were simply elongated tetraglyphic while the other 19were diglyphic and probably not dividing at all. (Table I). The tetraglyphic state (Figure 3A) The earliest modification of the actino­ probably arises just prior to or during divi­ pharynx in the process of longitudinal fission sion. Of the 200 anemones sampled in the is a division of the aboral rim (Figure 2B). field, 187 were diglyphic, while 5 were mono­ This occurs along the plane of division at glyphic and 8 triglyphic. The mono glyphic appro ximately the same site as the widest sepa­ polyps averaged 1.0 ± 0.1 em s.d. diameter ration between mesenteries (Figure 3D) , per­ (fixed) while the triglyphic averaged 1.7 ± pendicular to the directive axis. The longest 0.3 em s.d. diameter. Neither the triglyphic mesenteries in this area do not connect to the nor the monoglyphic polyps were signifi­ actinopharynx at this level. There must be a cantly different in size from the diglyphic separation of the mesenteries from the actino­ ones (1.4 ± 0.5 ern s.d.), although the trigly­ phar ynx in this region, as well as the forma­ phic ones were larger than the monoglyphic tion ofa notch at opposite sides of the aboral (P < 0.05, Analysis of Variance and Student­ rim (Figure 2C). Later stages show that divi­ Newman-Keuls test, F = 3.17, method of sion of the actinopharynx (Figure 3B) pro­ Sokal and Rohlf 1969). Evidently, tetraglyphy gresses toward the oral end with a concu rrent is an uncommon state among nondi viding infolding of the aboral free lateral edges. The anemones while not at all uncommon during final result of this infolding is the fusion of division. It is quite possible that division of the free edges (Figure 3D) to form two com­ tetraglyphic polyps could result in either two plete actinopharynxes aborally while division diglyphic or one monoglyphic and one tri­ continues orally. This produces an inverted glyphic individual. Alternatively , triglyphic U-shaped structure as in Figure 2C. The individuals may be a developmental stage lead­ fusion of the free edges of the divided actino­ ing to the tetraglyphic condition. Their large pharynx does not usually begin before final size and the lack of postdivision triglyphic in-

. .'".~ FIGUR E3. Sections of Anthopleura e/egantissima du ring longitudinal fission (scale bar = I mm). A : a tetraglyphic individual in division. No te the four directive pairs (D) and the comple te actinophary nx. Section taken at mid­ actinopharynx level. B : A tetraglyphic individual in division showing the separation of the actinophary nx (A) as in Figure 2C. Same individual as in A with section taken at lower level of actinophary nx. C: A daughter individual resulting from division of a diglyph ic anemone. Note the single directive pair (D), the incomplete actinophary nx (A), and the formation of new mesenteries (N) in the division scar area as in Figure 2G. Section taken at mid-actin opharynx level. D: Division of diglyphic individual showing the separation of the actinophary nx and fusion to form two actinophary nxes (A1, A2) and the widening of the complete mesenterial endocoe ls (E) as in Figure 2£. Section at lower level of actinophary nx. Phot ograph s printed by placing sections in enlarger (no negative). Morphological Variability during Fission of the Sea Anemone-SEBENS 127 dividuals support this interpretation. Division eavernosa by McCrady (1859), for M etridium of diglyphic polyps almost always results in senile (= M. fimbriatum) by Torrey (1898), two monoglyphic individuals. This explains and by Parker (1899), and for Haliplanella the field population that consists of mostly (= Sagartia) luciae, Anemonia suleata, and diglyphic individuals with a few monoglyphic Anthopleura thallia by Stephenson (1929). It and triglyphic individuals. Tetraglyphic polyps has also been reported in several other genera, in division (1.5 ± 0.6 em s.d.) were only slightly including Anthopleura elegantissima (see Hand larger than diglyphic ones (1.2 ± 0.5 em s.d.) 1955; Davis 1962; Francis 1973a, b, 1976, (not significantly different by ANOVA). It 1979), although no details of the process may be that internal rearrangement of larger have been given. Fission is similar in all such polyps takes so long that it must be begun species and results in the production of two before division occurs. equal or slightly unequal individuals follow­ Sections of daughter individuals showed ing a division of the body in the longitudinal that they can be either monoglyphic or di­ plane (Francis 1976). glyphic (no triglyphic ones were observed) Transverse fission, the second distinct asex­ (Table 1). In the monoglyphic division prod­ ual method, has been described for Gonaetinia ucts, new directive pairs arise from the body prolifera and Aiptasia couchii by Stephenson wall in the division scar area and grow in­ (1929), for Anthopleura stellula by Schmidt ward to meet the actinopharynx. The process (1970), and for Fagesia lineata by Crowell and proceeds from the aboral to the oral end , Oates (1980). In this method, division is in the and a new siphonoglyph forms where the di­ transverse plane and superficially resembles rective mesenteries meet the actinopharynx. the process of strobilization in the Scyphozoa. Diglyphic daughter individuals have the two Of the three asexual methods, transverse fis­ siphonoglyphs situated approximately 60° sion is the rarest and has been studied the apart. There must be substantial mesenterial least. .rearrangement if such individuals are to re­ Basal fragmentation or pedal laceration, turn to symmetry, involving production of the third method, has been differentiated as new mesenteries opposite the division scar. two distinct types (Stephenson 1929). Tearing None of the sections showed a definite exam­ basal fragmentation occurs in Sagartia elegans ple of such rearrangement, and it may be that and Diadumene cineta. Small portions of the the asymmetry persists for a long time after pedal disc are separated by a tearing process division since it should not impair function. as the anemone moves and these develop di­ The division scar area is the center of re­ rectly into individual anemones. Basal frag­ organization where new mesentery pairs arise mentation by constriction occurs in S. laeerata from the body wall, from the aboral to the (Stephenson 1929) where portions ofthe pedal oral end . Several of the sections showed such disc form lobes that separate from the main rearrangement (Figure 3C) involving produc­ individual by constriction. Such fragments tion of up to six new mesentery pairs within then develop similarly to those resulting from the first few weeks after division. Externally tearing fragmentation. Cary (1911) described the division scar begins to develop verrucae the process of pedal laceration in Aiptasia within a month or less after fission. The new pallida, Aiptasia tagetes, Bartholomea annu­ scar is probably indistinguishable after 2 to lata, and Cylista leucolena, and Rawlinson 4mo. (1934) did so for Metridium senile. Torrey and Mery (1904), Hammat (1906), and others have described the internal development and DISCUSSION regeneration of naturally produced basal frag­ ments and those produced by experimental of sea anemones separation of portions of the pedal disc (see occurs by four distinctly different processes. reviews in Stephenson 1929, Chia 1976). The The first of these, longitudinal fission, has phenomenon of budding, common among been described for Bunodosoma (= Aetinia) the hydroids, has never been described in 128 PACIFIC SCIENCE, Volume 37, April 1983

the Actiniaria although incomplete basal diglyphic individuals. The three-dimensional fragmentation or the formation of a second conformation of the actinopharynx during oral disc as a result ofinjury or developmental division of A . elegantissima (Type II) is strik­ accident (e.g., in Metridium senile as shown by ingly different from any previously described. Torrey 1898, and by Parker 1899may give the Division is externally similar to that of H. appearance of budding. luciae, but actinopharynx division is concur­ Longitudinal fission is widely distributed rent with column division in H. luciae so that taxonomically among actiniarians, but its closure ofthe actinopharynx must occur after description has usually been superficial and separation of the two halves. Two complete external. Only the studies of Torrey actinopharynxes are never seen in section s of (1898), Parker (1899), Walton (1918), Davis H. luciae during division. In M etridium senile (1919), and Atoda (1954, 1976) have given and bermudensis division was thought serious consideration to the internal events. to proceed from the oral to the aboral end as The very complete study by Davis (1919) de­ did division of the actinopharynx, which was scribed both the process of fission and the seen as two complete tubes in the upper course of regeneration in the resulting indi­ portion of the anemone (Torrey 1898, Parker viduals using serial sections from Haliplan ella 1899, Walton 1918). It is thus similar to luciae at many stages of division. Torrey (1898) A. elegantissima in conformation but with the and Parker (1899) both dealt with a very few polarity reversed. These examples are prob­ specimens of M etridium senile, a species in ably developmental abnormalities that do not which specimens with two oral discs are only continue to divide the entire . New rarely observed. Asexual reproduction of directive mesenteries arise from the division Metridium is accomplished by pedal lacera­ scar area in daughter individuals ofH . luciae. tion (Hoffmann 1976, Shick and Hoffmann Old directive pairs divide in both M. senile 1980, Purcell and Kitting 1982); in fact, there and A . bermudensis. Division is thus through has been no subsequent evidence that longi­ at least one directive endocoel while it oc­ tudinal fission actually occurs in this species. curs through the endocoels of complete me­ Walton's (1918) study of A ctinia bermudensis senteries perpendicular to the directives in also involved few individuals; the species nor­ A. elegantissima. mally reproduces sexually (dioecious) and The less common form of longitudinal di­ broods the juveniles. Again, Walton's speci­ vision in Anthopleura elegantissima (tetra­ mens may have been developmental abnor­ glyphy, Type II) is a complex process in which malities. Ina study of the population dynamics most of the major internal reorganization is of Anthopleura xanthogrammica in Washing­ carried out prior to division of the body wall. ton (Sebens 1977, in press), I observed one in­ When the separation finally occurs, the two dividual with two fully formed oral discs in a daughter individuals have almost complete population of greater than 500 mapped in­ actinopharynxes, complete body walls, a fused dividuals . This individual (8 x 10em basal sphincter muscle, and two siphonoglyphs (in diameter) survived at least the 3 yr of the symmetric division). There is less rearrange­ study. Such individuals are thus very rare but ment necessary to return them to their former viable even in the field. symmetry than in Type I division. This may There appear to be two distinct modes of be important in larger individuals where re­ longitudinal fission in Anthopleura elegantis­ arrangement and regeneration could take sima differing as to the timing of production longer. It is still possible that the tetraglyphic ofnew directive mesentery pairs and siphono­ condition is not preparatory for division. The glyphs (Figure 4). Either the diglyphic polyp large fraction of apparently dividing indi­ tears itself in half with no prior internal rear­ viduals that were tetraglyphic (24 percent, rangement (as in Haliplan ella luciae studied Table I), when none were found in samples by Davis 1919 and Atoda 1954), leaving each from the field population, argues that it is, in half monoglyphic, or it first becomes tetra­ fact , associated with fission. glyphic and then divides to form two usually The more common form of division in

IOlOJ ' 4 t l "I ,f Morphological Variability during Fission of the Sea Anemone-SEBENS 129

METRIDIUM SENILE

ACTINIA BERMUDENSIS

HAll PLANELLA LUCIAE A. ELEGANTISSIMA

ANTHOPLEU RA E LEGANTISS 1M A TYPE II

FIGURE 4. Rearrangement during longitudinal fission of three sea anemones. Partial division of a mono glyphic M etridium senile (Torrey 1898)occurs with separation ofthe directive mesenteries and formation ofa new member of each pair (dotted lines). Such abnormalities divide the oral disc and upper column but probably never go on to divide the entire anemone. In Actinia bermudensis (Walton 1918), a diglyphic individual divides with a similar separation of each pair of directives and formation of new members for the pairs . Division of both species occurs oral to aboral. Haliplanella luciae (Davis 1919)and Anthopleura elegantissima divide perpendicular to the directive pairs and new pairs are formed in each daughter rather than new members for each pair (Figure 2). In the second type of division of Anthopleura elegantissima, a new pair of directives arises in each halfprior to division such that the polyp is tetraglyphic while it isdividing (Figure 3A, B). Division ofthe latter two species occurs aboral to oral. Only the directive mesenteries and new directives (dotted lines) are shown. Other new mesenteries also arise in the area of the new directives. 130 PACIFIC SCIENCE, Volume 37, Apr il 1983

Anthopleura elegantissima is identical with Patterns and adaptive radiations. Pages that of Haliplanella luciae in most respects. 261-270 in G. O. Mackie, ed. Coelenterate The latter divides rapidly and must then spend ecology and behavior. Plenum Press, New a considerable amount of time in reorgani­ York. zation during which its normal behavior is CROWELL, S., and S. OATES. 1980. Meta­ impaired. Since the major internal structures morphosis and reproduction by transverse of the Actiniaria are similar for most species, fission in an edwardsiid anemone. Pages it is surprising to find such a diver sity in the 139-142 in P. Tardent and R. Tardent, process of splitting in two. However, natural eds. Developmental and cellular biology selection may work differently on such fac­ of coelenterates. Elsevier/North Holland tors as the length oftime involved in division, Biomedical Press , New York. the length of the regenerative period, and the DAVIS, C. 1962. One equals two : A sea anem­ postural condition of the anemones during one achieves its plurality in singular fash­ fission. Since the anemones studied to date ion. Nat. Hist. 71 :61-63. live in very different habitat types, it is not DAVIS, D. W. 1919. Asexual multiplication suprising that the problem of division has and regeneration in Sagartia luciae Verrill. been solved in several different ways. The two J. Exp. ZooI. 28: 161-263. modes of division in A . elegantissima may be FRANCIS, L. 1973a. Clone specific segregation characteristic of different habitats, seasons, in the sea anemone A nthop leura elegantis­ energetic states, or simply initial individual sima. BioI. Bull. 144:64- 72. size; these possibilities will be explored in - - - . I973b. Intraspecific aggression and future studies. its effect on the distribution of Anthopleura elegantissima and some related sea anem­ ones. BioI. Bull. 144: 73-92. ACKNOWLEDGMENTS - - - . 1976. Social organization within clones of the sea anemone Anthopleura I thank R. Cloney and D. Christiansen elegantissima. BioI. Bull. 150:361-376. for advice and instruction on microtechnical - --. 1979. Contrast between solitary and methods and C. Hand, R. T. Paine, and clonal lifestyles in the sea anemone Antho­ A. Siebert for helpful discussion. R. Cloney pleura elegantissima. Amer. Zool. 19: 669­ suggested the negative direct printing tech­ 681. nique used in Figure 2. I also thank the De­ FREDERICKS, C. A. 1976. Oxygen as a limiting partment of Zoology and the Friday Harbor factor in phototaxis and in intraclonal Laboratories ofthe University ofWashington spacing of the sea anemone Anthopleura for the use of space and equipment. elegantissima. Mar. BioI. 38 :25-28. HAM MAT, M. L. 1906. Reproduction ofMetri­ dium marginatum by fragmental fission . LITERATURE CITED Amer. Nat. Boston 40: 583-591. ATODA, K. 1954. The development of the sea HAND, C. 1955. The sea anemones of central anemone, Diadumene luciae, reproduced California. Part II. The endomyarian and by the pedal laceration. Sci. Rep. Tohoku mesomyarian anemones. Wasmann J. Biol. Univ. , Ser. IV BioI. 20 : 123-129. 13:37-99. - --. 1976. Development of the sea anem­ HOFFMANN , R. J. 1976. Genetics and asexual one Haliplanella luciae. V. Longitudinal reproduction ofthe sea anemone M etridium fission and the origin of mono-, di-, and senile. BioI. Bull. 15I :478-488. tri-gl yphic individuals. Bull. BioI. Stat. JOHNSON, L. L., and J. M. SHICK. 1977. Effects Asamushi 15: 133-146. of fluctuating temperature and immersion CARY, L. R. 1911. A study of pedal lacera­ on asexual reproduction in the intertidal tion in Actinians. BioI. Bull. Woods Hole sea anemone Haliplanella luciae (Verrill) in 20:81-108. laboratory culture. J. Exp . Mar. BioI. Ecol. CHIA, F. S. 1976. Sea anemone reproduction: 28 : 141-149.

4# !# ipt: * ! * fl ·ifieere:e'ffifW¢1t! iifi&#f@i$JR!ffiffi!!tH'tma Morphological Variability during Fission of the Sea Anemone-SEBENS 131

K IENER, A. 1971. Contribution a l'ecologie, SEB ENS, K. P. 1977. Habitat selection, repro­ la physiologie et l'ethologie de l'actinie du ctive ecology, and the control of body Diadumene luciae (Verrill). Bull. Soc. ZooI. size in two intertidal sea anemone popu­ France 1971: 581-603. lations, Anthopleura xa nthogrammica and MCCRADY, J. 1859. Instance of incomplete A. elegantissima. Ph.D. Thesis, University longitudinal fission in Actinia cavernosa. of Washington, Seattle. Pages 275-278 in Vol. I of Proc. Elliot. - --. 1979.The energetics ofasexua l repro­ Soc. Nat. Hist. , Charleston, S. C. duction and colony formation in benthic MINASIAN, L. L., Jr. 1976. Characteristics of marine . Amer. ZooI. 19:683­ asexual reproduction in the sea anemone, 697. Haliplan ella luciae (Verrill), reared in the - --. 1980. The control of body size and laboratory. Pages 289-298 in G. O. Mackie, longitudinal fission in the sea anemone ed. Coelenterate ecology and behavior. Anthopleura elegantissima (Brandt). BioI. Plenum Press , New York. Bull. 158: 370- 382. - --. 1979. The effect ofexogenous factors - -- . 1981a. The allometry of feeding, en­ on morphology and asexual reproduction ergetics, and body size in three sea anemone in laboratory cultures of the intertidal sea species. BioI. Bull. 161: 152-171. anemone, Haliplanella luciae (: - - -. 1981b. Reproductive ecology of the Actiniaria) from the coast of Delaw are. intertidal sea anemones Anthopleura xan­ J. Exp. Mar. BioI. Ecol. 40 :235-246. thogrammica (Brandt) and Anthopleura ele­ - - -. 1982. The relationship of size and gantissima (Brandt): Body size, habitat , biomass to fission rate in a clone of the and sexual reproduction. J. Exp. Mar. BioI. sea anemone Haliplanella luciae (Verrill). Ecol. 54: 225- 250. J. Exp. Mar. BioI. Ecol. 58 : 151-162. ---. 1982a. Asexua l reproduction in An­ MINASIAN, L. L., JR., and R. N. M ARISCAL. thopleura elegantissima (Brandt) (Anthozoa: 1979. Cha rac teristics and regulation of fis­ Actiniaria): Seasonality and spatial extent sion activity in clonal cultures of the cos­ of clones. Ecology 63 :434- 444. mopolitan sea anemone Haliplanella luciae - --. 1982b. Recruitment and habitat se­ (Verrill). BioI. Bull. 157: 478-493. lection in the intertidal sea anemones MIYAWAKI, M . 1952. Temperature as a fac­ Anthopleura elegantissima and A . xa ntho­ tor influencing upon fission in the orange­ grammica. J. Exp. Mar. BioI. Ecol. 59: 103­ striped sea anemone, Diadumene luciae. 124. J. Fac. Sci. Hokkaido Univ., Ser. IV, Zool. - - -. In press. Population dynamics and II: 77-80. habitat suitability ofthe intertidal sea anem­ PARKER, G. H . 1899. Longitudinal fission ones Anthopleura elegantissima (Brandt) in M etridium marginatum Milne-Edwards. and A . xanthogrammica (Brandt). Ecol. Bull. Mus. Compo Zool. Harvard 35 :901­ Monogr. 919. SHICK, J. M. 1976.Ecological physiology and PURCELL, J. E., and C. L. KITTING. 1982. genetics of the colonizing actinian Hali­ Intraspecific aggression and population planella luciae. Pages 137-146 in G . O. distribution of the sea anemone M etridium Mackie, ed. Coelenterate ecology and be­ senile. BioI. Bull. 162:345- 359. havior . Plenum Press, New York. RAWLINSON, R . 1934. A comparati ve study of SHICK, J. M., and R. J. HOFFMANN. 1980. M etridium senile L. var. dianthus (Ellis) and Effects ofthe trophic and physical environ­ a dwarf variety of this species occurring in ments on asexual reproduction and body the River Mersey, with a discussion on the size in the sea anemone M etridium senile. systematic position ofthe genus Metridium. Pages 211-216 in P. Tardent and R. J. Mar. BioI. Assoc. U.K. 19: 901-919. Tardent, eds. Developmental and cellular SCHMIDT, H. 1970. Anthopleura stellula (Acti­ biology of coelenterates. Elsevier/North niaria: ) and its reproduction by Holland Biomedical Press, New York. transverse fission. Mar. BioI. 5 :245- 255. SHICK, J. M., and A. N. LAMB. 1977. Asexual 132 PACIFIC SCIENCE, Volume 37, April 1983

reproduction and genetic population struc­ Sagartia davisi. Univ. Calif. Publ. Zool. ture in the colonizing sea anemone Hali­ 1 :211 -226. planella luciae. BioI. Bull. 153 :604-617. UCHIDA, T. 1932. Occurrence in Japan of SMITH, N. , and H. M . LENHOFF. 1976. Regu­ Diadumene luciae, a remarkable actinian lation of frequency of pedal laceration in of rapid dispersal. J. Fac. Sci. Hokkaido a sea anemone. Pages 117-126 in G. O. Univ., Ser. VI Zool. 2 :69-82. Mackie, ed. Coelenterate ecology and be­ --- . 1936. Influence of the currents upon ha vior. Plenum Press, New York. the distribution of races and frequency SOKAL, R . R ., and F. J. ROHLF. 1969. Bio­ of asexual reproduction in the actinian, metry : The principles and practice ofstatis­ Diadum ene luciae. Zool. Mag. Tokyo 48 : tics in biological research. W. H . Freeman 895-906. and Company, San Franciso. 776 pp. WALTON, A. C. 1918. Longitudinal fission STEPHENSON, T. A. 1929. On methods of re­ in Actinia bermudensis Verrill. J. Morph. production as specific characters. J. Mar. 31 :391 -406. BioI. Assoc. U.K. 16: 131-172. WILLIAMS, R. R 1973. Are there physiological TORREY, H . B. 1898. Observations on mono­ races ofthe sea anemone Diadumene luciae? genesis in M etridium. Proc. Calif. Acad. Mar. BioI. 21 :327-330. Sci., Ser. 3, Zool. 1 :345-360. ---. 1975. Catch-tentacles in sea anem­ TORREY, H. R , and J. R. MERY. 1904. Re­ ones: Occurrence in Haliplan ella luciae generation and non-sexual reproduction in (Verrill) and a review ofcurrent knowledge. J. Nat. Hist. 9 :241 -248.