A COMPARATIVE STUDY OF THE CLONAL AND SOLITARY FORMS OF THE SEA ANEMONE ANTHOPLEURA ELEGANTISSIMA The sea anemone Anthopleurd elegantissimg is referred to as the aggregating anemone of the middle intertidal region with an average column diameter of 1.5 inches by Ricketts and Calvin (1968 ed.). This description overlooked solitary occuring individuals of A. elegantissimg (Hand 1955), which I have found to have a vertical distribution that extends subtidally and a pedal disc diameter up to 15 cm. Prelimingry field observations suggested to me that there are two distinct forms of A. elegantissimg, an aggregating form and a solitary form. Distinctive features of the two forms include whether the anemone occurs in a dense clonal aggregation created by asexual reproduction (Francis 1973-a) or as solitary individuals, size, vertical distribution, and habitat. This study had the following objectives: 1) To examine the differences between the clonal and solitary forms, 2) To determine if the differences are genotypic or pheno¬ typic, and 3) To determine if there are any controlling influences on the occurence or expression of one form over the other. GENERAL MATERIAL AND METHODS This study involved the protected rocky intertidal zone (Ricketts and Calvin 1968 ed.) at Hopkins Marine Sta¬ tion and Pt. Pinos in Pacific Grove, Californig. All field observations and laboratory animals were collected from these areas. The following definitions of clonal anemones (hereafter clonal) and solitary anemones (hereafter solitary) were used in this study. Clonal was defined as any anemone failing to show aggression (Francis 1973-b) to a minimum of one near neighbor or having the characteristic scar and shortened tentacles indicative of recent fission. A solitary was defined as any anemone which did not meet either criterig of clonal. The anemones used in the laboratory studies were collected by carefully removing them from the rock substrate with a spatuld or fingernails. Anemones were allowed to settle in glass or plastic containers with a continuous flow of sed water at approximately 13?C. Nonclonemates and solitary anemones were kept separate to prevent aggression (Francis 1973-b). Anemones were not fed during the study, Methods used in comparing the clonal and solitary were; 1) Tissue grafting to determine tissue compatibility, 2) Starch gel electrophoresis for isozymes, 3) Morphological studies of nematocysts, 4) Field observations of distribution and habitat, and 5) Measurements of surface and mass. Each method and its results is treated in a separate section. METHODS AND RESULTS Tissue grafts To determine if there is a difference in tissue compa¬ tibility between the clonal and solitary forms, two methods of tissue grafting were employed using the following crosses: 1) Self to self, 2) Nonclonemate to nonclonemate, and 3) Clonal to solitary. The first method involved culturing tissue sections, The anemones were relaxed in an isotonic MgCly solution and strips of body wall approximately 10mm X 4 mm X 1 mm were excised from the pedal disc and column. Tentacle sections were prepared by excising a whole tentacle. clipping 1 mm of the tip to remove the aggression receptors (Francis 1973-b), then slitting one side to produce a sheet of tissue in a pie wedge shape. The two tissue pieces were placed side by side with both ectodermal surfaces facing the same way and the long cut edges in contact. This arrange¬ ment was held firmly between two frames supporting 1 mm nylon mesh which allowed circulation of water over the tissue, The frames were incubated in running sea water at about 13 for 7 days. In this manner, 1 series of pedal disc grafts, 1 series of column grafts, and 2 series of tentacle grafts were prepared. Grafts were evaluated after 7 days using the following criterig, fusion was characterized by the tissue sections remaining intact along 50% of the graft seam and rejection was characterized by anything less than 50%. The results showing 100% rejection for all crosses and tissue types are presented in Table 1. Problems encountered with the first method were tissue necrosis and muscular action within the tissue which dis¬ rupted the edges in contact. Attempts to correct these problems were made in the second method of tissue grafting, In the second method, halves of anemones were used instead of tissue sections and the halves were stitched together to maintain contact between the cut edges. The anemones were relaxed in an isotonic Mgcly solution, then cut longitudinally in half. For each cross, halves of simi¬ liar size were paired. The column halves were sewed together with square knots at 6 mm intervals using a curved needle and cotton thread. The grafts were incubated in running sed water at approximately 13'C. Two grafts were prepared for each of the three possible crosses using this method, The same definitions of fusion and rejection were used as in the first grafting method. Table 2 shows that after 7 days, rejection was observed in all crosses. The events leading to the rejection are similiar to asexual division (Davis, 1972). The halves pinched into two autonomous animals and moved away from each other. Local necrosis ground the stiches enabled the thread to cut through the softened tissue freeing the anemone halves as they separgted. Results for both grafting methods showed no differential grafting response among the three crosses. The common event observed was rejection. Isozymes Since electrophoresis for isozymes allows direct visuglization of the gene products, this technique was used as a measure of the genetic difference between clonal and solitary A. elegontissima. The method used was Brewer's (1970) vertical starch gel electrophoresis for esterase. Tissue extracts were prepared from mesenterial filaments of five clonal and five solitary A. elegantissimg. As an interspecies and intragenus comparison, two A. xanthogram¬ mica were also run. The mesenterial filaments were excised, blotted of excess moisture and homogenized in a ground glass hand homogenizer. The homogenate was centrifuged at 10,000 g for 10 minutes and the liquid supernatant used in the electrophoresis. Electrophoresis was carried out for 5 hours at 150 volts and 10 milliamps in a 3°C cold room following Brewer's (1970) procedure for the esterase system. The gel was sliced and stained for acid phosphatase activity (Shaw 1970) and esterase activity (Brewer 1970). Acid phosphatase activity was located in a faint band common to both clonal and solitary A. elegantissimg and the A. xanthogrammicg. These results indicated the similigrities within the genus Anthopleura and did not resolve any genetic differences within the species A, elegontissimg. Results for the esterase activity are shown in Figure 1. The A. xanthogrammica has one intermediate band which makes its esterase activity pattern distinctly different from the multi-banded pattern of the A. elegantissimg. The clonal and solitary A. elegantissimg have a common fast band, but show some variance in the two slower banding positions. These two slow banding positions have the characteristics of one locus with either a homozygous allele resulting in one band or a heterozygous allele resulting in two bands, the variation between the clonals and solitaries in the two slower banding positions is genetic, the differences can be attributed to any of the following: 1) The clonals and solitaries have two different loci, 2) It is the same locus, but different alleles, or 3) The esterase activity is an inducible isozyme. Support for this last reason of induci¬ bility is seen in slot 14 where a clonal has a slow band at a position similiar to a solitary's slow band. This clonal animal has a pedal disc diameter of 8 cm which is more common of solitaries than clonals. Morphology Nematocysts were used as the morphological charac¬ teristic to compare clonal and solitary, since it is a taxonomic feature used in the classification of seg gne¬ mones (Hand 1955). Nematocysts types were identified and percentages of the different types determined for the mesenterial filaments and tentacles. For the nematocyst study of the mesenterial filaments, six clonals and five solitaries were used. A piece of mesen¬ terial filament was placed on a glass slide and squashed firmly with the coverslip yielding a slide with identifiable unfired and fired nematocysts resolvable with a light micro¬ scope. Nematocyst types within random fields were counted until a total of 200 nematocyst were identified. The following classifications by Hand (1955) were used to divide the nematocysts into four groups: 1) Short basitrich 9.0-18.5 X 1.5-2.0 u, 2) Large basitrichs 25.0-39.0 X 3.5-6.0 u, 3) Thin basitrichs 27.0-48,0 X 0.5-1.5 u, and 4) Microbasic p-masti¬ gophores 11.0-27.0 X 2.0-4.5 u and 18.5-47.5 X 3.5-4.5 u. The results are compiled in Table 3. There is some indication that clonals have a greater percentage of small basitrichs and a lower percentage of large basitrichs than solitaries, (p slightly greater than 0.05 using Student t test), Nematocysts of the tentacles were studied in five clonal and five solitary. The method involved snipping the tip of the tentacle and treating this piece of tissue in the same manner as the mesenterial filament preparation. Nematocysts were counted until 100 were identified. The nematocysts were classified as either spirocysts 9.0-29.0 X 1.5-3.0 u or basitrichs 14.0-24.5 X 2.0-3.0 u (Hand 1955). Results are summarized in Table 4 and show that the clonals have more spirocysts relative to basitrichs than the solitaries (p less than 0.05, Student t test). To determine if the nematocyst frequencies are affected by the size of the anemone and not necessarily its identity as clonal or solitary, the nematocysts in the tentacles of a clone containing varying sizes of animals were examined, Nematocyst counts of tentacles were taken for two gnemones at each 1.2 cm increment in pedal disc sized from 2.5 cm to 8.8 cm. Figure 2 shows that as the pedal disc size increases the relative number of spirocyst decreases (r - 0.89, p is less than O.01). Field observations Field studies were conducted to answer such questions as the difference in vertical distribution and habitat that exist between clonal and solitary. The distribution of the clonal was from 2,5 m in exposed greas with strong wave action to ,6 m above mean lower low water level, while the solitary were found from 1.2 m to subtidal depths. In studying the clonal and solitary habitats the zone of coexistance became a focus point. A salient relationship was noted in surge channels in which both solitaries and clonals were found. These surge channels ranged in width from 10 to 50 cm and were of yarying widths, a typical surge channel is illustrated in Figure 3. Solitary anemones were found more frequently at the mouth of these channels than within the channel. The reverse rela¬ tionship was seen for clonals. Twelve surge channels were observed and anemones scored according to whether clonal or solitary, and whether at the mouth or within the channel, This data is summarized in Table 5 and shows a preferential diestribution of solitary at the mouth and clonal within the channel. Another feature of the surge channel habitat appegred to be a size gradient as a function of distance from the channel mouth. Five surge channels were observed. Measure¬ ments of pedal disc size of both solitaries and clonals were made. Locations of the anemones measured were 15 cm apart extending from the mouth to a distance of 45 cms. The pedal disc size of the anemone was plotted against its distance from the channel mouth in Figure 4. The data fit a linear regression (r = 0.87, and p is less than 0.01). It is apparent that as the distance from the mouth increased, the pedal disc size decreased, Variations in size within a clone were noted for several clones occuppying surge channels or vertical faces. The clonal members negrest the surge channel mouth or at the lowest position on a vertical surface approached the size of solitary anemones. Data for this gradient of size as a function of distance from the mouth was collected from 4 clones along surge channels. Pedal disc megsurements of the anemones were taken at locations of 10 cm increments from the mouth to a distance of 30 cm into the channel. Results gre graphed in Figure 5 and show a linear increase in pedal disc size as the distance from the mouth decregses (r = 0.84, and p is less than O.01). The sizes of animals within clones on sloping surfaces were measured as a function of vertical height for four clones. The lowest clonals were considered O with the rest of the clone's position relative to this marker. Measurements of the anemones' pedal disc size were taken gt locations 10 cm apart, from O to 30 cm in vertical height. The results are graphed in Figure 6 and show a linegr increase in pedaldisc size as the vertical height decregses (r = 0.73, p is less than O.01). Surface to mass relationships The morphology of the clonal and solitary anemone was studied further by computing the following surface to mass measurements: 1) Tentacle grea per mass, 2) Oral disc gred per mass, and 3) Exposed surface ared per mass. Five clondl and five solitary animals were used, and the data was obtained in the manner described below. Tentacle greas and oral disc greas were taken on anemones induced to expand in a dilute solution of the liquid supernatant from homogenized squid. For the tentacle greas, five tentacles were randomly selected from an anemone and the base diameter and length measured. Using the formuld for the surface area of a cone, the average surface gred per tentacle was determined. This value was than multiplied by the total number of tentacles to givethe total tentacle surface area for the anemone. The oral disc surfac gred 11 required an oral disc diameter measurement which was con¬ verted to area by the formuld for the grea of a circle, The exposed surface area was measured in submerged animals forced to contract by prodding them with a probe until no further contraction was noted. The surface gred of clonals was approximated as a half sphere since their columns are protected by clonemates. The half sphere gred was computed by using half the contracted column digmeter as the value for the radius. The solitary surface grea was approximated as that of a half sphere plus a cylinder equal to the exposed column. The method of weighing employed was reduced weight obtained by weighing the anemone suspended in sea water. The results are summarized in Table 6. The clonals have more tentacle grea, oral disc gred, and exposed grea per mass than the solitary, DISCUSSION The results showed differences between clonal and solitary in their isozyme activity, nematocyst frequencies, distributions, habitat, and in several measures of surface area to mass ratios. The variance in esterase activity and nematocyst per¬ centages are indicative of possible genetic differences between clonal and soiitary, however there is a strong possibility that both results are inducible by size. This influence is suggested by the large clonal with a solitary esterase banding pattern. Clearer support for size influence 12 was the decrease in tentacle spirocyst percentages with increasing anemone size within a single clone. Since the enzymes and nematocysts are an integral part of the feeding process, these features may be influenced also by diet and feeding behavior. There is not enough evidence to support genetic differences as maintaining the two distinct forms, The existance of the two forms if not genetic, suggests a phenotypic expression controlled by external forces, Hand (1955) and Francis (1973-a) attribute the solitary form to a more protected environment since its size is more vulnerable to wave shock. I also found solitgries in protected environments, but found them more frequently at the mouth of surge channels than clonals, a distribution pattern which may reflect differences in feeding habits, I postulate that in surge channels a solitary at the mouth is feeding on incoming food laden water, the water is depleted of some of it particles by the solitary and can support only smaller more efficient clonals further up the channel. The size gradient observed in clones along surge channels and vertical faces also fits this model. The anemones nearest the mouth or lowest in vertical height are feeding on the most food laden water and thus can grow larger per unit food gathering greg. The genetic variation of esterase activity and nema¬ tocysts are also compatible with the model since they dre involved in the feeding process and could be influenced by food availability. Of particular interest is that small clonals have more spirocysts than large solitaries. Spirocysts when discharged create a mesh of entangling fibers thought to be used in trapping prey (Mariscal 1974). It would be advantageous for the small clonal to have more spirocysts since they would be feeding on water relatively poorer in large pieces of food than the large solitary, The morphological surface areas to mass can be applied to the food availability scheme. Tentacle grea per mass is d measure of feeding efficiency, and the oral disc greg per mass is a measure of farming efficiency in providing sun¬ light for its algal symbionts. Thus the clonal form is a more efficient feeder and farmer than the solitary, which is in keeping with clonal's position in greas of possibly decreased food availability, This study best supports the model that solitary and clonal are phenotypic expressions controlled perhaps by food availability. The solitary individuals may be less efficient feeders and are found at surge channel mouths and at a lower tidal level than the clonals where the availability of large amounts of food may be greater. The small clongl is d more efficient feeder and farmer, and is a phenotype expressed when food availability is low. I wish to thank the faculty, staff and students at Hopkins Marine Station; particularly my advisor Nathan Howe for his endless help and encouragement, and Phil Murphy for his expertise with starch gel electrophoresis. SUMMARY Clonal and solitary forms of A. elegantissima were comparatively studied and found to have differences in isozyme activity, frequencies in nematocyst types, and intertidal location. These differences suggested that food availability was the determining factor in the distribution and expression of the two forms. 14 LITERATURE CITED Davis, D. 1962. One equals two: a seaanemone achieves its plurality in singular fashion. Nat. History 71(2): 61-63. Francis, L. 1973-a. Clone specific segregation in the sed anemone Anthopleurg elegantissimg. Biol. Bull. 144: 64-72. Francis, L. 1973-b. Intraspecific aggression and its effect on the distribution of Anthopleurd elegantissimg and some related sed anemones. Biol. Bull. 144: 73-92. Hand, C. 1955. The sea anemones of central Californig, Wasmann J. Biol. Part 2 13: 37-99. Mariscal, R. N. 1974. Nematocysts, p. 129-178. In Muscatine and Lenhoff (eds.), Coelenterate biology: reviews and new perspectives. Academic Press, N.Y. 501 p. Ricketts, E. F., and J. Calvin. 1968. Between Pacific Tides 4th ed., rev. by J. W. Hedgpeth, Stanford University Press. TABLE CAPTIONS Table 1: Grafting results using the first method of tissue sections. Table 2: Grafting results using the second method of stitching gnemone halves together, Table 3: Numbers of each nematocyst type counted per 200 total nematocysts in the mesenterial filaments of 6 clonals and 5 solitaries. Nematocyst types designated by A, B, C, and D are: A) Small basitrichs, B) Large basitrichs, C) Thin basitrichs, and D) Microbasic p-mastigophores. Numbers of spirocysts and basitrichs per 100 Table 4: nematocysts counted in the tentacles of 5 clonals and 5 solitaries. Table 5: Precentages of the number of clonals and solitgries situated at the mouth and within the channel of surge channels. Surface area to mass ratios for 5 clonals and 5 Table 6: solitaries. e COMBINATION SELF TO SELF NONCLONEMATE TO NONCLONEMATE CLONAL TO SOLITARY TABLE 1 TISSUE TYPE PEDAL DISC COLUMN TENTACLE PEDAL DISC COLUMN TENTACLE PEDAL DISC COLUMN TENTACLE % REJECTION 100 100 100 100 100 100 100 100 100 SAMPLE SIZE 1 1 1 COMBINATION SELF TO SELF NONCLONEMATE TO NONCLONEMATE CLONAL TO SOLITARY TABLE 2 % REJECTION 100 100 100 SAMPLE SIZE 2 S.D. 115 126 92 104 105 72 102.3 18.75 B 40 28 72 58 48 52.3 17.49 TABLE 3 CLONAL A D C 25 100 20 42 90 15 22 62 16 72 35 16 64 32.7 78.6 12.2 19.26 7.33 15.81 SOLITARY B C 73 10 70 84 83 84 78.8 7.4 2.80 6.76 D 17 32 38 42 35.2 10.34 X S.D. NUMBER OF SPIROCYST 57 66 56 68 60.4 6.11 TABLE 4 CLONAL NUMBER OF BASITRICH 43 34 44 32 45 39.6 NUMBER OF SPIROCYST 52 57 49 50 50.6 1.14 SOLITARY NUMBER OF BASITRICH 48 49 50 49.4 S.D. X S.D. CLONAL n=286 % CLONALS % CLONALS AT MOUTH IN CHANNEL 98% TABLE 5 SOLITARY n=26 % SOLITARY % SOLITARY AT MOUTH IN CHANNEL 81% . 2 5 . ON o a oN 0 o 1 S 99 + 0 0 0 Figure 1: Figure 2 Figure 3: Figure 4: Figure 5 Figure 6: FIGURE CAPTIONS Starch gel electrophoresis stained for esterase activity. Tissue extracts are from the mesenterial fildments of 5 clonal and 5 solitary A. elegantissma, and 2 A. xanthogrammicg. Two clonal anemone tissue preparations were run in duplicate and the identical results combined as seen in slot 1 & 2. and slot 5 & 6. Graph showing decrease in the percentage of tentocle spirocysts as function of increasing size, represented by pedal disc diameter. Sample size is 10 gnemones from the same clone. Illustration of a typical surge channel, Size of gnemone determined by pedal disc diameter as a function of distance from the mouth of a surge channel. Data obtained from solitgries and clonals at 12 surge channels, Variation in size of clonals as a function of distance from the mouth of a surge channel. Data was collected from 4 clones along surge channels. Variation in size of clonals as a function of location on a vertical surface. The lowest clonal member is 0, with vertical heights being relative to this marker. Data was obtained from 4 clones along vertical surfaces. — — e LE L LE 2 L D C e SIskooulas Q e 1 + — L L L LL — eo NId — LE CHANNEL FIGURE 3 MOUTA 83 LE FIG. 10 000 SOLITARY CLONAL OO O 45 30 DISTANCE FROM MOUTH IN CM 60 — L FIG 4 2 DISTANCE O O 30 20 FROM MOUTH IN CM L FIG. O O 20 VERTICAL HEIGHT IN CM 30