Interspecific Aggression Page 1 INTRODUCTION The sea anemones Anthopleura elegantissma (Brandt,1835), Metridium senile (Verrill, 1865), and Corynactis californica (Carlgren, 1936) associate sympatrically on the pilings under the Monterey wharf. Anthopleura elegantissma is a west coast anemone. In- tertidally, it is found from about -2.0 to +4.5 feet above mean lower low water level. (This is the clonal variety) Metridium senile is a circumpolar, temperate to cold water anemone found on both coasts. It can be found as high as +3.0 feet above mean lower low water level. It also occurs well below tide marks. Corynactis californica is found along the Pacific coast north of the equator. It is most profuse at the mean lower low water level and below. On the pilings I have observed interspecific separation lines approximately 1.5 inches wide between A. elegantissma and M. senile. Interspecific separation lines about 1 inch wide have also been found between A. elegantissma and C. californica. Childress (1969) has demonstrated that the inter-clonal Interspecific Aggression Page 2 separation lines (Francis, 1973a) found between A. elegantissma clones are formed and maintained by intra-specific aggression. Presented is a report on the interspecific aggressive behavior of the three above mentioned sympatric sea anemones and its relation to the observed interspecific separation lines. MATERIALS AND METHODS Collecting and field studies were carried out on the first eight rows of pilings after the Marina boundary, at Pier 2, Monterey wharf. Field observations and studies were con¬ ducted using SCUBA gear. In the case of A. elegantissma and M. senile a spatula was utilized to collect specimens (Francis, 1973a) I used a hammer and chisel to chip offthe Balunus nubilus shells and their attached Corynactis. This minimized damage and provided experimental animals on a movable substrate. The species of anemones were kept separately in tanks that were supplied with flowing sea water at about 13°C. The anemones were fed Tigropus califoricnus intermittently except during experiments when food was withheld. PROCEDURES, OBSERVATIONS AND RESULTS Intra-specific Aggression Francis (1973b) has shown intra-specific aggression between different clones (Francis, 1973a) of A. elegantissma. This does not seem to be the case with regard to M. senile and C. californica In the lab, utilizing the procedure outlined below, I never Interspecific Aggression Page 3 observed aggression between colormorphs of these two species. Furthermore, in the field, no intraspecific separation lines were noted in either M. senile or C. californica. Interspecific Aggression To ascertain the dominance hierarchy order, the follow- ing procedure was utilized (same procedure used in intraspecific aggression). Procedure: 1) An anemone was settled in a finger bowl and its position marked on the outside of the bowl. 2) An interspecific antagonist, settled on a movable substratum would be brought within contact distance. 3) After a day the outcome of the aggressive event could usually be determined. Movement away from the confrontation and/or visible necrosis were the factors used in assessing the outcome. M. senile was the most sucessful interspecific aggressor, followed by C. californica. A. elegantissma turned out to be the least dominant aggressor. These findings and their stat¬ istical significance are listed in Table 1. e tadte i he Aggression and the maintenance of interspecific separation lines To determine whether aggression was a major factor main- taining separation lines, the following experiments were performed. Procedure: 1) Three dissecting pans (8x111.5 inches) were layered with a white wax bottom. 2) Each pan was filled with a different binary combination of the three species. The animals were pinned to the wax so that the initial aggregation patterns were fixed. 4 Interspecific Aggression Page 4 3) The two different species were separated by a zig-zag pattern boundary made up of microscope slides glued together. The pattern maximized border anemone contact. 4) After three days the pins and boundary were removed. 5) Dead or unattached anemones were removed to simulate field conditions. The experiment was run for two weeks. Net movement at the borders confirmed the results of the individual interspecific aggressive confrontations. M. senile pushed back the A. elegantissma border and killed the C. californica border anemones. A. elegantissma retreated from the Corynactis border. A stable border with no contact between neighboring species was established by the two weeks. Aggressive behavioral pattern of A. elegantissma The interspecific aggressive pattern exhibited by A. el egantissma is identical to its intraspecific behavioral pattern described by Childress (1969). This behavior can be separated into six stages: 1) Stimulation, which involves repeated tentacle contact and withdrawal; 2) Inflation, when the acrorhagi become turgid; 3) and 4) the Movement of Inflation and Movement of Application, during which the acrorhagi move towards the victim; 5) Application of Ectoderm, during which acrorhagi are applied; and 6) Recovery, when the anemone returns to its normal posture. Aggressive behavioral pattern of C. californica The term "aggressive" is misleading when used to describe Interspecific Aggression Page 5 C. californica. Defensive response would be the more correct terminology. I have never observed C. californica initiate interspecific aggression. When attacked, it will retract its tentacles, shorten its column and contract the sphinctor at the top of the column. Close examination will disclose a minor extrusion of some mesenterial filaments thru the mouth. If not attacked again, C. california will regain its normal posture in a matter of hours. However, if attacked again, it will fully extrude its mesenterial filaments onto the aggressor. This behavior will usually cause the interspecific antagonist to retract and/or retreat. I have not seen the capitate tentacles actively used in aggression by C. california. Aggressive behavioral pattern of M. senile Upon tentacular contact with an interspecific antagonist M. senile partially retracts its tentacles in the local region of stimulation. It then elongates its body column and bends toward the victim. During this period, all the tentacles that face the victim are extended and then applied to it. M. senile does not withdraw after tentacle application. Usually it is the victim that breaks contact and initiates avoidance behaviors such as leaning away, retracting the column, or physically moving away. Approximately 70% of the time, M. senile will initiate aggressive behavior before its interspecific antagonist. Interspecific Aggression Page 6 Receptor location To find the location of the receptors that detect in¬ terspecific antagonists, the following experiments were performed. Procedure: 1) Tentacles were snipped off all three species of anemones and used as probes to touch different parts of an interspecific antagonist. 2) As a control, a clonemates tentacle was used to see if the anemone would discriminate between self and non-self. 3) A positive response was assumed if the subject retracted its tentacles and/or signs of aggressive response followed. Childress (1969) found that an excised A. elegantissma tentacle was still completely effective in eliciting aggress¬ ion after many (greater than 10) contacts. This observation was found to be true also with M. senile and C. californica tentacles. Metridium and Corynactis did not respond to stimulus by their own species, while Anthopleura would respond to a non- clonemate. All three species of anemones also did not respond to an interspecific tentacle if touched anywhere other than the tentacles. If touched elsewhere and at the tentacles, retraction occured. Furthermore, Anthopleura and Metridium responded only if contact was at the tentacle tip. On the other hand Corynactis responded only if contact was along the tentacle sides. I would assume that the receptors that detect Interspecific Aggression Page 7 interspecific antagonists are located in these respective areas. Light intensity and anemone distribution Hand (1955) noted that the Corynactis colonies under the Monterey wharf occurred on pilings where there was no direct sunlight. I have found colonies in my study site exposed to direct sunlight, but these colonies have an upper limit approximately 3 feet lower than the Corynactis found under H the wharf in the shadows. (Figure 1) Light meter readings taken May 28 ", 4:30 pm, show a four-fold decrease in foot-candles from the outermost to the innermost pilings, the latter being in constant shadows. Thus, there is a positive correlation between decreasing light intensity and higher Corynactis distribution. The same type of correlation, but to a lesser degree, holds for Metridium. On the other hand, regardless of piling position, the A. elegantissma colonies in my study site always were spread down to the upper limit of the Corynactis or Metridium colony below it. It would seem then that light intensity is not a major factor limiting Anthopleura distribution on the pilings. I have observed that within my study site, Metridium and Corynactis occupy different microhabitats, i.e. they do not occupy the same piling. I have observed two pilings that have both Metridium and Corynactis settled on it, but the interspecfic separation lines are over two feet wide. Page 8 Interspecific aggression Preliminary Observations have observed that M. senile will secrete abnormal amounts of mucus when disturbed, such as in aggression. Tigropus califoricnus coated with Metridium mucus survive the entire test period (10 seconds) when placed on the tentacles of an A. elegantissma. In contrast, uncoated Tigropus are instantly killed when placed in the same situation. Both the coatéd and uncoated Tigropus are instantly killed when placed on the tentacles of a C. californica. DISCUSSTON As I have noted before (Intro.) the range of A. elegant- issma can extend down to -2 feet below mean lower low water. Furthermore, I have found solitary A. elegantissma living at -52 feet. Yet on the wharf pilings, both varieties are restricted to a narrow range delineated at the low- er limit by interspecific borders shared with either Metridium or Corynactis. This fact, coupled with the border experiments and dominance hierarchy experiments, indicate that the distribution of A. elegantissma has been limited by interspecific aggression with Metridium and Corynactis. In turn, there is evidence that environmental factors such as light prevent Metridium and Corynactis from extending their upper limit of distribution. Other environmental Page 9 Interspecific Aggression factors such as dessication, food supply and wave action undoubtably have some influence on anemone distribution. The reasons for the aggressive superiority of Metridium are not immediately obvious. However, my preliminary observations point out the possibility that the mucus secreted by Metridium could protect it against Anthopleura. This protection could be in the form of an anesthetic inhibiting the firing of nematocysts. Another possibility is that the mucus serves as a protective coating against Anthopleura or Corynactis. Corynactis feeding" response Lang (1971 and 1972) noted interspecific aggression in Scleractinian coral, which are of the order Madreporaria. She observed that when Scolymia lacera was brought into contact with Scolymia cubensis, the former would extrude its mesenterial filaments and digest the tissue of the latter. Lang (1971) describes this act of aggression as basically an extracoelenteric feeding response. This behavior is remarkably similar to the interspecific aggressive pattern of C. californica, a member of the Order Corallimorpharia. In Hyman (1940) the Madrepores are reported as readily derivable from Corallimorphidae. If so, this would indicate that the receptors that detect interspecific aggressors are linked to the normal extracoelenteric feeding behavioral pattern in C. californica. Interspecific aggression Page 10 SUNARY The sea anemones Anthopleura elegantissma, Metridium senile, and Corynactis californica are observed to engage in interspecific aggression. This aggressive behavior is elicited only thru tentacle contact. The receptors that detect interspecific antagonists are located only on the tentacle tips in Anthopleura and Metridium, while Corynactis detects from the sides of its tentacles. Metridium and Corynactis were found to occupy different microhabitats at the field site. I did not observe inter- specific aggression between them in the field. I did observe interspecific aggression in the field between Anthopleura and Metridium, and Anthopleura and Corynactis. Interspecific separation lines can be set up by inter¬ specific aggression, in the lab. Each species of anemone exhibits an aggressive behavioral pattern peculiar to its own species. Anthopleura elegantissma has morphological structures called acroraghi used specifically for aggression. Corynactis californica extrudes mesenterial filaments in a manner similar to its extracoelenteric feed- ing response when attacked. Metridium senile may produce mucus during aggression as a self-protective mechanism. Interspecific aggression and environmental factors such as light intensity influence the distribution of sea anemones on the pilings under the Monterey wharf. Interspecific aggression Page 10b ACKNOWLEDGEMENTS I wish to thank Nat Howe for his helpful advice. I am indebted to all my diving buddies for getting this project into the water. Special thanks go to Chuck Baxter forhelpfully tearing my paper apart, and making it better each time. Page 11 Interspecific Aggression LITERATURE CITED Childress, L., 1969. Intra-specific aggression and its relation to the distribution pattern of the clonal sea anemone Anthopleura elegantissma. Ph. D. thesis, Stanford University, 123 pg. Francis, L., 1973a. Clone specific segregation in the sea anemone Anthopleura elegantissma. Biol. Bull., 144:64-72 Francis, L., 1973b. Intraspecific aggression and its effect on the distribution of Anthopleura elegantissma and some related sea anemones. Biol. Bull., 144:73-92 Hand, C., 1955. The sea anemones of central California, Part I. The Corallimorpharian and Athenarian anemones. Wasman J. Biol., 12:345-375 Hyman, L. H., 1940. The Invertebrates: Protozoa through Ctenophora. First edition. McGraw-Hill Book Company, Inc. Lang, J., 1971. Interspecific aggression by Scleractinian corals. 1. The rediscovery of Scolymia cubensis (Milne Edwards and Haime). Bull. of Mar. Sci., 21(4):952-959 Lang, J., 1973. Interspecific aggression by Scleractinian corals. 2. Why the race is not only to the swift. Bull. of Mar. Sci., 23(2): 260-279 terspeific Aggression TABLE DOMINANT AGGRESSOR TYPE OF ENCOUNTET C.c. A.e. M.s. A. elegantissma vs. M. senile — A. elegantissma vs. -- 2 californica californica Vs. M. senile Draw PæO.05 PO.01 Pæ0.025 5 5 5 3 + + 5 2 — 5 3 S 2 r — c Interspecific aggression Record of able I aggressive confrontations ividual inte: Page 0 Interspecific aggression Page 13 FIGURE CAPTIONS Figure L. Vertical distribution of the three major sympatric sea anemones at the wharf, Anthopleura elegantissma(A.e.), Metridium senile (M.s.), and Corynactis californica (C.c.). Absolute depth was obtained using the tidal guage kept by the Naval Postgraduate School at Pier 2.