Begle Page 2 ABSTRAC Leptasterias hexactis (Stimpson 1862) shows a patchy distribution a¬ long the rocky intertidal of south Monterey Bay. It was found that the population density increased linearly with an increasing amount of avail¬ able shelter. Starfish are found either under rocks or algal thalli, due mainly to a strong negative phototaxis. Possible major factors behind this phototaxis are visual predation and desiccation, and ob¬ servations suggest that visual predation is primary. Lepasterias in shaded conditions tolerates exposure at low tide where there are no a¬ vian predators. The population at Pt. Pinos exhibits a high level of cryptic coloration which is proposed to result from visual predation. In the Hopkins Marine Station preserve, where populations of potential predators wer highest, the stars occur in very low density. Food items of Leptasterias were examined at Pt. Pinos and under the Cannery and were found to be radically different both from each other and from previous work done in Puget Sound. In addition, escape responses were described for six local gastropods in the presence of Leptasterias. Tricolia pulloides showed the strongest response, with Mitrella tuberosa and Littorina scutulata exhibiting moderate responses. Barleeia haliotiphila and L. planaxis showed weak responses, and Bit- tium eschrichtii showed virtually no response to either chemoreception or contact with a starfish tube foot, even though Barleeia and Bittium are important food items. Begle page 3 General Introduction The midtidal region of much of the rocky outer coast of central California is a dense algal turf community dominated by Gigartina pap illata and Rhodoglossum affine. This turf community has a complex mesofaunal association of small worms, arthropods, and molluscs liv¬ ing within it which are coextensive with the standard array of more familiar midtidal animals. A question of particular interest con¬ cerns the potential predators on the mesofauna, with one important can¬ didate being the predatory asteroid Leptasterias hexactis (Stimpson 1862). Much taxonomic confusion has resulted from the tremendous var¬ iability of Leptasterias, and what have been variously classified as L. hexactis, L. aequalis, and L. pusilla are now included by Chia (1966) in the single species, Leptasterias hexactis. In the Monterey Bay area there are two distinct extremes of morphological forms, but the gradations between these are innumerable, and for the purposes of this study, all were considered to be L. hexactis. Extensive feeding studies have been recorded for Leptasterias in ... the Puget Sound region (Menge 1970). Leptasterias generally moves up with the tide to forage, and if prey is captured that is too large to consume during high tide, or too late to finish consumption before low tide, the starfish will move down with the prey item to finish consump¬ tion over low tide. Little quantitative work has been done in the cen¬ tral California area, especially in this midtidal community, but some incidental observations by Smith (1971) indicated some of the midtidal Begle Page 4 mesofauna as possible prey. Some escape responses to Leptasterias have been described for and various larger gastropods; Notoacmaea scutum,AColisella limatula (Phillips 1976), Colisella pelta (Margolin 1964), and Tegula funebralis (Yarnall 1963), but little mention has been made of escape or avoid¬ ance behavior of some of the smaller gastropods occurring commonly in the midtidal mesofauna of central California. This study was begun in part to fill in the gaps in the local diet of Leptasterias, and to examine some of the escape and avoidance responses of local mesofaun¬ al gastropods. Although Leptasterias occurs widely from central California to Puget Sound, there is considerable patchiness along the small section of coast at the south end of Monterey Bay. Observations were made to try and discern the physical or biotic factors that might be affect¬ ing this occurrence in microhabitat, and to try and compare their rel¬ ative importance. Description of the study sites Three sites were chosen, one for its obvious lack of Leptaster¬ ias, the others for their abundance. Point Pinos Located at the south end of Monterey Bay, is exposed out- er coast. Ocean swells and large waves contribute to very active wat¬ er conditions. The area consists of granitic reef with some large boulders, making up twenty to thirty meters of exposed intertidal. Abrupt variations in height from one to two meters are not uncommon. The entire area is covered with thick algal growth. Major represent¬ Begle Page 5 atives other than the two main turf algae are Iridaea flaccida, Pel¬ vetia fastigiata, Fucus distichus, Gigartina canaliculata, and Egreg- ia menziesii. Mussel Point Situated inside Monterey Bay as part of the Hopkins Marine Station preserve, is a much more sheltered area. It receives only direct swells from the northwest and refracted swells from the south. The area is composed of the same granitic substrate, and con¬ sists mostly of rock outcroppings (4-5 meters) and boulders (1-2 met¬ ers). Smaller, broken-up rocks are less abundant and scattered. The intertidal zone is much narrower, extending from ten to fifteen met¬ ers out to the water. Algal growth is much less dense, and approxi¬ mates the densities encountered at Pt. Pinos only in small isolated patches. Hoyden Cannery Consists of an approximately four by five meter ti¬ dal flat under the shelter of the abandoned Hovden Cannery building. Although the area did not contain much algae, the high densities of starfish present warranted observation of the mysical conditions and the local diet of Leptasterias. In essence, the area most closely resembles an under-rock or even subtidal location, with the constit¬ uent fauna mostly tunicates, sponges, hydroids, and barnacles. II Methods Field Studies: An area at Pt. Pinos with a relatively high density of Leptasterias was studied in detail. Extensive sampling was done within this area using randomly placed .25 square meter quadrats. In each quadrat was recorded the number of Leptasterias, number of Lepta¬ Begle Page 6 sterias feeding, food items, and a subjective estimate of the percent of the quadrat area usable as shelter by starfish. Observations were also made of the conditions of Pt. Pinos and Mussel Pt. at high and low tides on both calm days and days with large surf. Mussel Point was sampled using . randomly placed ten meter long transects, scoring one meter on either side of the line, resulting in a twenty square meter sample area. Estimates of the percent shelter were obtained using a .25 square meter quadrat, again placed randomly. Owing to the small size of the area under the Cannery, it was possible to sample the entire area at low tide. In addition to the quadrat studies, many feeding observations were made at Point Pinos over a five week period from mid-April to late May. Records were kept of the number of starfish seen, number feeding, and the number of each food item observed. Escape Responses For the chemoreception studies the 25 snails to be tested were placed in each of two large glass bowls, filled with 100 ml. of fresh sea water and allowed to settle for approximately one half-hour. Eight milliliters of fresh sea water was then pipetted in, with both bowls serving as their own controls. Responses of the snails were ob¬ served for twenty to thirty minutes. For the experimental runs, eight milliliters of sea water was pipetted in from a bowl in which 8 to 10 Leptasterias had been held for one hour. (Average wet weight of indivi- dual Leptasterias 3.5 grams) The behavior of the snails in each ex¬ perimental bowl was compared both to its own control run and the du¬ le Page 7 plicate run simultaneously. Two sets of control runs and two sets of experimental runs were done for each species. For Tricolia pulloides additional tests were run in a plastic tub in which Gigartina papil- lata fronds were place such that the response on the algal thallus could be observed. A similar protocol was followed, with fifty snails on each plant, and each set of snails serving as its own control. Some studies were done on the responses of the same species of snails to contact with Leptasterias tube feet, using fifty individu¬ als of each species (40 for Bittium eschrichtii). The snail to be tested was placed in a glass bowl filled with 75 milliliters of fresh sea water, then allowed to come into contact with a clean probe. Be¬ havior was observed through a dissecting microscope. After five to ten minutes, the same snail was allowed to make contact with a tube foot held in fine forceps and subsequent behavior observed and com¬ pared with the control. III Results Results of a sampling program showed dramatic differences in the density of Leptasterias in the rocky intertidal at the south end of Monterey Bay. Sampling done at Mussel Point had on the average .1 starfish per square meter. A favorable habitat at Point Pinos showed a density of 6-7 per square meter, while the area under the old Hov¬ den Cannery building had a density of 9-10 per square meter in an ap¬ proximately 25 square meter area. It was observed that close to twenty percent of the animals found at Pt. Pinos had lost from one to five arms, and were in the process Page 8 of regeneration. Essentially all of the Cannery specimens were whole and undamaged. It was also found that the color of the stars at Pt. Pinos would match that of the substrate up to eighty percent of the time. Those at the Cannery were many bright shades, and not cryptic with respect to their background. Measurements were made of the percent of each quadrat area usable as shelter. Figure 1 shows this percentage, plotted against the num¬ ber of animals per quadrat for fifty randomly placed quadrats in the zone inhabited by Leptasterias at Pt. Pinos. The number of animals can be seen to increase linearly with increasing available shelter, with a positive slope of 0.678. There is some scatter, but the line obtained from a least-squares linear regression analysis is signif¬ icant (p.001). Similar measurements were obtained from the quadrats placed at Mussel Point, where the mean shelter per quadrat was approximately twenty percent. Feeding Figure 2 shows that at Pt. Pinos the small gastropod Barleeia haliotiphila is the preferred prey item, in terms of total number of prey items observed in that area, comprising 53 percent of the diet. Tricolia pulloides, another small gastropod, ranks second, comprising 21 percent. In none of the feeding observations was the snail in its shell swallowed, in fact in some cases up to three or four Barleeia would be digested simultaneously outside the body. Other important prey items included Bittium eschrichtii, seven percent, Tegula fune¬ Begle Page 9 bralis, four percent, and two observations each of Notoacmaea insessa and Margarites sp. One observation was made of a starfish consuming Mopalia lignosa. Unidentified soft tissue made up eight percent of the total. Under the Cannery, the feeding differed widely from that at Pt. Pinos. The primary food items were the barnacle Balanus glandula (367) and a small unidentified juvenile nestling pelecypod, perhaps Hiatella (367). Next was the smaller barnacle Chthamalus dalli (167). Under the shade of the Cannery building, individuals were observed exposed on rock surfaces feeding on both species of barnacles when the tide was out.(40% of individuals). One observation of feeding on the snail Mitrella tuberosa was made here, the only such observation during the course of this study. Again, eight percent of the observations were of unidentifiable soft tissue. Escape Responses Tricolia pulloides This species showed the strongest response, both at a distance and to contact (see Fig. 3) with over 90% of all experimental animals responding (Fig. 4). Onset of the distance response was almost im¬ mediate for all snails responding, withethe response lasting approx- imately twenty minutes. Distance response involved an increased lo¬ comotion rate, increased rate of beating of cephalic and epipodial tentacles, and climbing. In both bowl and frond tests all of the re¬ sponding snails immediately ceased normal behavior of slow movement with frequent turns and exhibited fast unidirectional movement, along Page 10 with the other aspects of the response. If possible, snails will leave the water, and if not on an algal frond when this occurs, they will eventually die of desiccation on the lip of the experimental bowl or tub. Those on fronds will return to the water after a two to three hour interval. Contact evokes essentially the same behavior, except that the in- itial direction of locomotion is directly away from the point of stimula¬ tion. Contact with the cephalic tentacles caused retraction of the anterior portion of the body and reversal of the direction of locomo¬ tion. Contact with the side of the foot or epipodial tentacles caused a violent throwing of the shell away from the stimulus, with uninter- rupted fast locomotion and a turn at approximately a right angle away from the point of stimulus. Contact with the rear of the foot caused the foot to be withdrawn momentarily, with immediate resumption of locomotion. The operculum was closed only when the snail was in¬ verted and the tube-foot place in continuous contact with the soft parts. Littorina scutulata Response to chemoreception involved increased unidirectional lo¬ comotion and climbing, although not as strongly as Tricolia. Unlike Tricolia, the response does not cease after leaving the water, result- ing in large masses of ten to twenty snails precariously crawling on the lip of the experimental bowl. Contact evokes similar behavior, with upwards of 90% responding (Fig. 4), except that the initial direction of locomotion is directly le Page 11 or at an acute angle away from the stimulus, with subsequent climbing. No difference was seen in the response when contact with the tube foot was made with other parts of the body, except that contact with the posterior portion of the foot caused momentary retraction of that por- tion and uninterrupted locomotion, as in Tricolia. Mitrella tuberosa M. tuberosa showed a highly variable, but moderate (see Fig. 3) response at a distance, consisting of a brief burst (about 5 min.) of locomotory activity with no consistent direction shown. No climbing was observed. These are unusually active snails to begin with, and a considerable number of control animals would show a response, how¬ ever the experimental response was significantly higher, as Fig. 4 shows. Contact involved rapid retraction of the siphon or tentacles, rear¬ ing up on the posterior portion of the foot, change in direction, and increased locomotion away from the stimulus. Contact with the clean probe did not induce the siphon or tentacles to be withdrawn nearly as quickly. Littorina planaxis L. planaxis showed no appreciable response by distance chemore¬ ception, as the number responding to the control was not significantly different from the experimental situation. (Fig. 4) Contact with a tube foot evoked a slow turn and slightly increased locomotion away from the point of stimulus. The response was highly variable in terms of speed of retreat and angle of turning. Begle Page 12 Barleeia haliotiphila B. haliotiphila showed essentially no response by distance chemo¬ reception, as Fig. 4 shows. The response to contact involved a shallow turn away from the stimulus and slightly increased rate of locomotion. The response was variable both in occurrence and intensity, and was weak overall. No climbing behavior was ever observed. Bittium eschrichtii This was the only snail to show virtually no response to either contact or distance chemoreception, as Figure 4 clearly shows. Begle Page 13 IV Discussion Originally, the question of Leptasterias' habitat choice arose when initial observations at Mussel Point indicated a very low densi¬ ty of Leptasterias relative to Pt. Pinos. Though the two areas seem similar, closer study revealed major differences between them relating to available cover. The density of Leptasterias at Pt. Pinos increases linearly with the amount of available shelter (rocks or large fronds of macroalgae). Leptasterias shows a consistent negative phototaxis (Menge 1972) which, when coupled with the tidal cycle of vertical movements accounts for the preference for such shelter during daytime low tides. Major reasons postulated for this response include avoidance of desiccation and visual predation (Menge 1970) and both of these factors would be at maximum levels during daytime low tides. Some estimate of the relative importance of these two factors in determining microhabitat occurrence may be made from comparison of the populations at Pt. Pinos and under the Cannery for the following fac¬ tors: % at Cannery % at Pt. Pinos Less than 17 1) Stars with damaged rays 20% damaged 80% cryptic 2) Color match to substrate Low % 40% out Less than 17 3) Exposed on rocks at low tide Taken together, these indicate a lower level of predation at the Cannery than at Pt. Pinos. Birds are not seen feeding or resting on Begle Page 14 rocks under the Cannery, and since algae is virtually missing, the turf- feeding surfperches which are possible predators (Nichols 1979) are unlikely to forage there. Casual observations on birds indicates reas¬ onable populations of shorebirds on the rocks at Pt. Pinos, and there is no reason to assume fish are not resident in normal numbers. There is also indicated strong selection for cryptic coloration in the Pt, Pinos population. This species would be very labile in its response to such selection since it broods eggs and the young recruit to the local population. The facts that Leptasterias tolerates mild exposure under the Cannery and that the species possesses the behav¬ ior of being able to follow the tide up and down makes it appear that desiccation is unlikely to be a strong determinant in microhabitat oc¬ currence compared to the effects of predation. Returning to the original question of the virtual absence of Lep¬ tasterias from Mussel Pt., we can apply the relationship of percent cover to density plotted in Figure 1 for Pt. Pinos. Using this as a model for prediction of a population density at Mussel Pt., where available shelter averages twenty percent, we would predict a density of two Leptasterias per .25 meter square. The observed density is two per twenty square meters, and if we follow our above argument that des¬ iccation is not a strong force in population regulation, then predation must be expected to be very high in this habitat. This could well be the critical factor in explaining the very low density of Leptasterias at Mussel Pt., where the densities of shorebirds (Braslow 1979) are probably higher than any site in south Monterey Bay, as are those of fish (Miller and Geibel 1973). Begle Page 15 This study shows that at Pt. Pinos a small gastropod identified as Barleeia haliotiphila was the main prey species, followed by Tri- colia pulloides. Smith (1971) noted that a small gastropod he iden- tified as Diala (Barleeia) acuta was the main dietary item of Lepta- sterias, but kept no quantitative records. Since I have worked in the same area without encountering this species it is probable that he was referring to B. haliotiphila. Under the Cannery, the barnacle Balanus glandula was a major food item, along with a juvenile pelecypod (Hiatella?), and the smaller bar- nacle Chthamalus dalli. These differences in dietary items reflect somewhat the differences in the sites themselves; a shaded, flat area with slight algal growth and little surf versus a rocky zone with dense algae and high wave exposure, inasmuch as the density of gastropods is determined by the density of algae and local water conditions. The extensive study done by Menge (1970) listed two barnacles, Balanus glandula and B. cariosus as the main dietary items, followed by some limpets; Acmaea (Notoacmaea) scutum and Acmaea (Colisella) pel¬ ta, and finally some smaller gastropods such as Lacuna sp., Littorina scutulata, and Margarites sp. The only similar food species observed in Monterey Bay were the barnacle B. glandula and the snail Margarites sp. A considerable percentage of small gastropods comprise the rest of the diet, both in Monterey and in Puget Sound, although the constituent spec¬ ies differ radically. It is interesting to note that the small gas¬ tropod Barleeia haliotiphila has no counterpart in the diet at Puget Sound. This indicates Leptasterias is a species with plastic feeding habits, which was to expected, given the varied dietary items catalogued Begle Page 16 by Menge. When escape or avoidance responses are observed in the lab, it is important to keep in mind the natural context in which they occur. Tricolia is usually found on algae such as Gigartina papillata, and since Leptasterias is most likely to approach from below, the negative geotactic response it exhibits to asteroid scent is highly adaptive. One possible result of this action, desiccation, is apparently more desirable than risking predation, although opportunities to leave the water in the field may be limited depending on the state of the tide and the location of the particular algal thallus. Littorina scutulata also consistently leaves the water, favoring desiccation (to which it is very well adapted) to possible consumption. In the case of Mitrella tuberosa, the brief burst of locomotory ac¬ tivity is apparently enough to carry it away from a foraging Leptas¬ terias without exposing the snail to harmful environmental conditions. Littorina planaxis, congener of L. scutulata, is usually out of the water already and shows only a weak response to contact stimulation, not surprising considering they are unlikely to encounter each other in the field. Barleeia is usually found on similar algal types as Tricolia, and its lack of any strong response, coupled with its high abundance in the intertidal, probably contribute to its being the main dietary item for the Pt. Pinos population. Bittium eschrichtii remains an enigma, showing no escape or avoidance behavior, and it is puzzling why it should be left evolutionarily bereft of such re¬ sponses. Begle Page 164 Acknowledgement. I would like to thank all of the staff of the Hopkins Marine Sta- tion for making this all possible. Most of all I want to thank Robin Burnett for his sense of humor and insight, and my advisor Chuck Bax¬ ter for his patience and quiet wisdom. Begle Page 17 Literature Cited Braslow, J. 1979. The effects of guano deposits on the adjacent in¬ tertidal community. (Unpublished MS. on file at Hopkins Marine Sta¬ tion Library). Chia, Fu-Shiang. 1966. Brooding behavior of a six-rayed starfish, Lep- tasterias hexactis. Biol. Bull. 130(3):304-315. Margolin, A. S. 1964. A running response of Acmaea to seastars. Ecol¬ ogy 45:191-193. Menge, B. A. 1970. The population ecology and community role of the predaceous asteroid, Leptasterias hexactis (Stimpson). Ph.D. Thesis. University of Washington. 213 pp. University Microfilms, Ann Ar- bor, Mich. —. 1972. Foraging strategy of a starfish in relation to actual prey availability and environmental predictability. Ecol. Monogr. 42:25-50. Miller, D. J., and Geibel, J. J. 1973. Summary of blue rockfish and lingcod life histories; a reef ecology study; and giant kelp, Macro- cystis pyrifera, experiments in Monterey Bay, California. Fish Bull. Calif. No. 158. 137 pp. Nichols, A. 1979. Predation by tidepool and nearshore fishes and its impact on the rocky intertidal zone community. (Unpublished MS. on file at Hopkins Marine Station Library). Phillips, D. W. 1976. The effects of species-specific avoidance res¬ ponse to predatory starfish on intertidal distribution of two gas¬ tropods. Oecologia 23:83-94. Smith, R. H. 1971. Reproductive biology of a brooding sea-star, Lep¬ Begle Page 18 tasterias pusilla (Fisher), in the Monterey Bay region. Ph.D. The- sis. Stanford University. 214 pp. Yarnall, J. L. 1963. The responses of Tegula funebralis to starfishes and predatory snails. Veliger 6 (Suppl.):56-58. 8 . *o 0 (O O 0 .. O 0 Naavoo and GHAAZSSO SIVNINV Begle Page 19 8 8 8 8 10 0 0 Barleeia haliotiphila Tricolia pulloides Bittium eschrichtii Tegula funebralis Notoacmea insessa Margarites sp. Mopalia lignosa Miscellaneous Balanus glandula Unident. pe lecypod Chthamalus dalli Mitrella tuberosa Miscellaneous Begle Page 20 % PT. PINOS FOOD ITEMS % CANNERY FOD ITEMS a 0 0 . 35 Begle Page 21 1dX OAINOS 1 2 1 Z 1 2 00 Z 10 L OOS OOO ONIGNOSSZA INBSaad 1 7 2 O 0 2 — O 2 Z Z Begle Page 22 Begle Page 23 Captions to Figures Eig. 1) Percentage of each .25 meter“ quadrat usable as shelter plot- ted against the number of Leptasterias seen in that quadrat. N-48 y= 0.678x + 0.57 p .001. Fig. 2) Dietary items for Pt. Pinos and Cannery. Shown as a per- centage of the total number of items at each site. Pt. Pinos - N=426 Cannery - N=62. Fig. 3) Animals tested for avoidance and escape responses to Lep¬ tasterias. ++ - Strong response + - Medium response + - Weak response — - No response. Fig. 4) Percentage of each species responding to escape response tests. Top- Percents responding to contact with Leptasterias tube foot. Bottom- Percents responding to distance chemoreception of starfish scent.