Selective predation by the mosshead sculpin Clinocottus globiceps on the sea anemone Anthopleura elegantissima and its two algal symbionts

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1 fomia. 3. Breakdown of stratification and biogeochemical response to overturn. Limnol. Oceanogr. 38: PATTEN, D. T, AND OTHERS The Mono Basin ecosystem: Effects of changing lake level. National Academy Press. ROMERO, J., AND J. M. MELACK Sensitivity of vertical mixing in a large saline lake to variations in runoff. Limnol. Oceanogr. 41: STINE, S Late holocene fluctuations of Mono Lake, eastern California. Palaeogeog. Palaeoclimatol. Palaeoecol. 78: VORSTER, I? A water balance forecast model for Mono Lake, California. Earth resources monograph. Forest Service Region 5, USDA. WILLIAMS, W. D The worldwide occurrence and liminological significance of falling water-levels in large, permanent saline lakes. Verh. Intemat. Verein. Linmol. 25: Received: I1 April 1997 Accepted: 4 November 1997 Limnol Oceanogr.. 43(4). 199x, 71 l by the Amencan Society of Limnology and Oceanography, Inc. Selective predation by the mosshead sculpin Clinocottus globiceps on the sea anemone Anthopleura elegantissima and its two algal symbionts Abstract-The mosshead sculpin Clinocottus globiceps (Girard, 1857) feeds on the sea anemone Anthopleuru elegantissima that contains two different algal endosymbionts, zooxanthellae and zoochlorellae. During laboratory feeding experiments, the sculpin selectively fed o-n the tentacles of zooxanthellate anemones over those of zoochlorellate and algae-free anemones. Zoochlorellae passed through the fish gut unharmed while zooxanthellae were degraded. The productivity of zooxanthellae in the fish feces ( pg C celll h-l) was significantly lower (93% less) than that of zooxanthellae freshly isolated from anemones ( pg C celll h-l), whereas the productivity of fecal zoochlorellae was the same as that of freshly isolated zoochlorellae ( pg C cellll h-j). The chlorophyll content (Chl a and c) of zooxanthellae was reduced by 50% after passage through the fish gut while the chlorophyll content of zoochlorellae (Chl a and b) did not change. Selective predation on zooxanthellate anemones confers several ecological advantages to zoochlorellate anemones and to zoochlorellae, most notably predator avoidance and dispersal of viable zoochlorellae that may serve as a source of symbionts for other anemones. By influencing the outcome of predator-prey interactions involving their hosts, symbiotic algae may have broader ecological roles in benthic communities than previously described. The sea anemone Anthopleura elegantissima is an ecologically important member of the rocky intertidal community, occurring on the North American Pacific Coast from Alaska to Baja California, Mexico (Hand 1955). Photosynthesis by zooxanthellae (Symbiodinium californium) in this anemone contributes substantially to primary production of the rocky intertidal zone in southern California (Fitt et al. 1982). Besides dinophyte zooxanthellae, anemones in the northern part of the anemone s range harbor green chlorophyte algae known generally as zoochlorellae (Muscatine 1971; O Brien 1978). Zooxanthellae and zoochlorellae symbionts occur in both A. elegantissima and its congener A. xanthogrammica (O Brien 1978). Anemones that harbor mostly zoochlorellae are green, anemones with mostly zooxanthellae are brown, and anemones that lack algae are white (algae-free or non- symbiotic). All three types, as well as mixed anemones containing both zooxanthellae and zoochlorellae, are found in the vicinity of one another in the Puget Sound region (pers. obs.). The primary role ascribed to symbiotic algae is provision of photosynthetic carbon to the animal host (Muscatine 1990). Carbon budgets derived for zooxanthellate and zoochlorellate A. elegantissima during summer months suggest that zooxanthellae are able to provide substantially more carbon to their anemone host than are zoochlorellae (Verde and McCloskey 1996). The presence of zoochlorellae in addition to zooxanthellae in anemones is puzzling if the only function of the algal partner is to provide photosynthetic carbon to the animal. Algal symbionts may have other roles in the symbiosis, especially in temperate regions, where anemone hosts may not rely on carbon provided by their symbiotic algae (Davy et al. 1997). A. elegantissima is an active carnivore that feeds on plankton and small invettebrates (Sebens 1981). The presence of two distinct algae in one host anemone allowed us to explore the possibility of multiple roles for symbiotic algae. In this study we determined that symbiosis with one or the other alga affects the outcome of predation on the host anemone. A variety of fishes and invertebrates, including the mosshead sculpin Clinocottus globiceps (Hand 1996; Yoshiyama et al ) the nudibranch Aeolidia papillosa (Waters 1973; McFarland and Muller-Parker 1993), and the leather star Dermasterias imbricata (Sebens 1977) consume both A. elegantissima and A. xanthogrammica. We consider whether the presence of one symbiotic alga or the other provides an associational defense (sensu Hay 1992) for the animal host. Associational defenses, where a palatable partner is protected by its association with an unpalatable species, have been described for seaweed-herbivore interactions (Hay 1992; Wahl and Hay 1995). If predation on the anemone host is influenced by its algal endosymbiont complement, the benefit of associating with the deterrent algal species will be significant when grazing pressure is high. We used intertidawtidepoo1 C. globiceps, which has the

2 712 Notes same geographical range as A. elegantissima (Eschmeyer et al. 1983) and is a visual feeder (Hand pers. comm.; Yoshiyama et al ). This sculpin consumes both A. elegantissima and A. xanthogrammica (Hand 1996), which comprise a significant part of its diet (Grossman 1986). We first determined that the mosshead sculpin selects its anemone prey on the basis of the presence of zooxanthellae and(or) zoochlorellae in the tentacles. We then measured the photosynthetic activity and chlorophyll content of zooxanthellae and zoochlorellae after passage through the fish digestive tract to determine the viability of these algae, since zooxanthellae have been shown to survive passage through the gut of both fish and nudibranch predators on tropical anemones (Muller-Parker 1984). The preference for zooxanthellate anemone prey suggests that zoochlorellae confer an associational benefit to their host. The presence and type of symbiotic algae in animal hosts are likely to affect predatorprey interactions in communities where symbiotic associations are abundant. Fish and anemone collection-three small tidepools (- 1.5 m in diam by I m in depth) were haphazardly selected during low tide (mean tidal level was m) on 16 July 1995 at Tatoosh Island, Washington (48 24 N, 124 4O W). Tidepools were half emptied before adding a few drops of quinaldine (an anesthetic) to the water. Forty-four mosshead sculpins (size range of mm total length) were collected using dip nets. The fish were transported to Shannon Point Marine Center (Anacortes, Washington) in buckets of seawater and were held in sea tables in a flow-through seawater system supplied with ambient seawater (12 C). The fish were fed the chlorophyte seaweed Ulva sp. ad libitum during a 2-week acclimation period. Anthopleura elegantissima was collected from Anaco and Shannon Point beaches. Anemones were removed from intertidal rocks using a blunt knife. The three representative types were collected and designated as either zooxanthellate, zoochlorellate, or nonsymbiotic after microscopic examination of clipped tentacle samples. The presence of 290% zoochlorellae or zooxanthellae in the tentacle clippings was used to assign anemones to one of these types. Microscopic examination of tentacles from white anemones confirmed that these anemones did not contain either alga in their tentacle regions. All anemones were maintained in ambient seawater in separate sea tables in the flow-through seawater system and were fed brine shrimp (Artemia sp. nauplii) each morning. Selection experiments-twenty-six individual mosshead sculpins were tested for anemone prey preference. Each fish was placed into a plastic mesh basket (36 X 25 X 17 cm in depth) that contained seven anemones arranged randomly (three zooxanthellate, three zoochlorellate, and one nonsymbiotic). The baskets remained submerged in the flow-through sea table. The anemones were placed into the baskets at 0600 h and allowed to attach before adding the fish at 1200 h. The mosshead sculpins and anemones were maintained together and supplied with running seawater for 6 h. Although the experiments were conducted in an enclosed facility, natural light was supplied by large glass windows. A 6-h period was deemed appropriate to allow the fishes to adjust to their surroundings and to feed on anemones. C. globiceps selectively grazes on tentacles over other body regions (Hand 1996; Yoshiyama et al. 1996a). Using a dissecting microscope, we counted the total number of each type (zooxanthellate, zoochlorellate, nonsymbiotic) of anemone tentacles eaten by each fish. The initial number of tentacles was independent of anemone type (ANOVA) and averaged 59 per anemone. Analysis of algae in fish feces and freshly isolated from host anemones-mosshead s&pins were randomly divided into two groups and placed into separate seawater tanks (22 per tank) supplied with running seawater. After a 48-h starvation period, one group of fishes was fed zooxanthellate anemones and the other group was fed zoochlorellate anemones. Fish fecal pellets were collected within 12 h and used for chlorophyll or radioactive carbon measurements. At the end of each day, the fish tanks were rinsed to remove all remaining fecal waste produced during that day. Fish fecal pellets (containing zooxanthellae or zoochlorellae) were collected on 3 to 4 consecutive days and used for chlorophyll analysis. Fecal pellets of each type were collected with a pipette (pooled fecal pellets from each tank on a given day constituted one sample). Each sample was gently filtered through 25-pm Nitex mesh to remove animal debris. The algal filtrate was diluted with 0.5-pm filtered seawater, and zooxanthellae and zoochlorellae cell densities were determined from the mean of six hemacytometer field counts. For each sample, four to six replicate subsamples were then filtered onto Whatman GFK 2.5-cm glass-fiber filters (-3 million cells per filter) and frozen for later analysis. Zooxanthellae and zoochlorellae were isolated from the tentacle regions of four other anemones of each type by homogenizing these tissues in filtered seawater and preparing algal samples from each anemone as described above. These freshly isolated algae served as controls for comparison to the algae from within the fish feces. Filters containing zooxanthellae were homogenized in 90% acetone, and filters containing zoochlorellae were homogenized in 100% methanol using a motorized teflon pestle tissue homogenizer. Homogenized filter slurries were allowed to extract in the dark in a refrigerator for 24 h. The samples were then centrifuged and the absorbance of the supematants read on a diode-array spectrophotometer. The equations of Parsons et al. (1984) were used to determine Chl a and c of zooxanthellae and those of Holden (1976) were used for Chl a and b of zoochlorellae. Individual fecal pellets for productivity measurements were collected (one fecal pellet presumably from one fish), passed through 25-pm Nitex mesh, and diluted as described above. Each pellet was treated as an individual sample for the radioactive carbon measurements, although for practical purposes the fishes fed one anemone type shared the same tank, which constitutes pseudoreplication (Hurlbert 1984). Fecal pellets were collected at 0900 h and incubated by 1100 h. One-milliliter samples of fecal algae were dispensed into 20-ml glass scintillation vials for light and dark treatments (dark vials were wrapped with electrical tape to exclude light). [ Clbicarbonate (I &i) was added to each sample.

3 Notes 713 Table 1. Comparison of the number of tentacles of zooxanthellate, zoochlorellate, and nonsymbiotic Anthopleura elegantissima consumed by the mosshead sculpin Clinocottus globiceps. The actual number of consumed tentacles from each anemone type is compared with the number of tentacles expected to be consumed if there was no selection by the fish (based on the ratio of anemone types presented to each fish: 3 : 3 : 1, zooxanthellate : zoochlorellate : nonsymbiotic anemone). The order of fish grazing preference on tentacles of anemones is zooxanthellate > zoochlorellate > nonsymbiotic anemone (n = 26 fish tested; G = 29.45, P < 0.01). Total tentacles consumed (C) Total tentacles expected to be consumed (E) Ratio C : E Zooxanthellate Zoochlorellate Nonsymbiotic anemone Total A loo-~1 subsample was removed from each vial for determination of total activity before incubating vials under an average photosynthetically saturating irradiance of pmol mm2 s-l (Muller-Parker unpubl. data) provided by a bank of cool-white fluorescent lamps suspended above a flow-through seawater tank (12 C). Incubations were terminated after 45 min and photosynthetic rates (pg C fixed cell ml h-l) calculated as in McFarland and Muller-Parker (1993). Photosynthetic rates of freshly isolated algae obtained from the tentacles of four individual brown and four green anemones were obtained in the same manner. Statistical analysis-we used a log-likelihood G-test (Zar 1996) to determine if the actual number of tentacles of each type consumed by C. globiceps deviated from that expected 9 I * r-1 Freshly Isolated Feces Chl a Chl c Chl a Chl b zooxanthellae zoochlorellae Fig. 1. Mean chlorophyll content of zooxanthellae and zoochlorellae isolated from their anemone host Anthopleuru elegantissima (freshly isolated) or obtained from feces of the mosshead sculpin Clinocottus globiceps fed A. elegantissima (feces). Error bars are + 1 SD (n = 4 for freshly isolated algae, 4 for fecal zoochlorellae, and 3 for fecal zooxanthellae). Zooxanthellae: *, P = for Chl a and P = for Chl c. to be consumed given the ratio of anemone prey provided to the fish. Our null hypothesis was that the fish did not select among anemone types and consumed tentacles in the ratio in which they were provided. The total number of tentacles (629) consumed during all trials and the ratio of anemone types provided in each trial (3: 3: 1, zooxanthellate: zoochlorellate : nonsymbiotic) were used to calculate the expected number of tentacles of each anemone type to be consumed if the fishes did not select among anemone types. We treated the results obtained from each fish (the number of tentacles of each type consumed) as a single sample and pooled the data for the 26 fishes. Because each fish was tested only once, our data are presented as a single experiment with 26 replicates. Chlorophyll and productivity data were analyzed using one-way ANOVAs to compare the chlorophyll content and productivity of freshly isolated algae with the chlorophyll content and productivity of fecal algae. Photosynthetic rates of fecal and freshly isolated algae were log-transformed to meet the assumption of homogeneous variances. Results and discussion-c. globiceps consumed tentacles from all A. elegantissima types (Table 1). However, mosshead sculpins showed a clear preference for tentacles of zooxanthellate anemones over those of zoochlorellate anemones, which were chosen with the second highest frequency. Nonsymbiotic anemone tentacles were least preferred by the fish (Table 1). During the 6-h trials with seven anemones available to each fish, the fish consumed an average of 7.3, 4.8, and 4.5% of the tentacles of a zooxanthellate, a zoochlorellate, and of a nonsymbiotic anemone, respectively. The chlorophyll content (Fig. 1) and photosynthetic productivity (Fig. 2) of fecal algae show that zoochlorellae pass unharmed through the fish gut, whereas zooxanthellae are degraded. Compared to zooxanthellae freshly isolated from A. elegantissima, the Chl a and c contents of algae isolated from mosshead sculpin feces are reduced by 40 and 60%. respectively (Fig. 1). Fecal zooxanthellae fixed only 7% of the carbon per cell fixed by freshly isolated zooxanthellae (Fig. 2). In comparison, the Chl a and b contents of freshly isolated and fecal isolated zoochlorellae are the same (Fig. l), and there was no significant difference between the productivity of fecal and freshly isolated zoochlorellae (Fig. 2).

4 714 NOfC!S 4.0 The different fates of zooxanthellae and zoochlorellae afi. j Freshly Isolated ter ingestion may reflect differences in the structure and 3.5 physiology of the two algae. O Brien (1980) showed that I Feces acid phosphatase activity is restricted to the surface of the 3.0 cell wall of zoochlorellae within the coelenteron of A. xanthogrammica, suggesting that zoochlorellae cell walls are resistant to lysosomal hydrolase activity. The composition and structure of the external coverings of zooxanthellae might make these algae more susceptible to lysis due to gastric acidity, or to the action of the mosshead sculpin digestive CSlZy lcs. As in seaweeds, where association with an unpalatable brown alga provides significant protection from herbivorous fishes for palatable green and red algae (Wahl and Hay 1995), anemones with zoochlorellae may benefit from the associational defense of reduced predation in the presence of anemone predators. The advantage of zoochlorellae in de i * T zooxanthellae zoochlorellae Fig. 2. Mean carbon fixation rates for rooxanthellae and zoochlorellae isolated from their anemone host Anthopleura elegantissima (freshly isolated) or obtained from feces of the mosshead sculpin Clinocottus globiceps fed A. eleganfissima (feces). Error bars are +l SD (n = 4 for freshly-isolated algae, 15 for fecal zoochlorellae, and 13 for fecal zooxanthellae). *, P < Direct comparison of the chlorophyll content and productivity of zooxanthellae and zoochlorellae (freshly isolated algae) shows that zooxanthellae contain more Chl a (Fig. 1) and are more than twice as productive as zoochlorellae on a cellular basis (Fig. 2). The algal endosymbiont complement of the anemone A. elegantissima affects its susceptibility to fish predation. Mosshead sculpins show a clear preference for anemones in the following order: zooxanthellate > zoochlorellate > nonsymbiotic anemone (Table 1). There arc several reasons why the mosshead sculpin might prefer to consume zooxanthellate anemones. Zooxanthellate anemones may be of greater nutritional value than zoochlorellate anemones because zooxanthellae translocate larger quantities of glycerol and other photosynthetic products to the animal tissue (Muscatine 1971; Trench 1971), or because zooxanthellae are degraded while zoochlorellae pass through the gut unharmed (Figs. 1, 2). Other factors that may influence the mosshead sculpin s choice include visual recognition, chemical cues released by the anemones, and taste preference. We are unable to distinguish among these possible factors. Observations by Hand (pas. comm.) and Yoshiyama et al. (19966) strongly suggest that the mosshead sculpin is a visual predator. The fishes prefer to eat tentacles over other anemone body regions (Hand 1996; Yoshiyama et al. 1996a). Hand (1996) found that tentacles of adjacent anemones may be protected by contraction, and proposed that contraction occurred in response to the alarm pheromone anthopleurine released in the vicinity by injured anemones. The conditions of our experiments (flow-through seawater; 6 h period) allowed sufficient time for reexpansion of anemones. terring grazing by C. &biceps would persist during winter months, when light limitation makes it unlikely that photosynthetic carbon fixed by either symbiont is able to meet the energetic requirements of the host. Conflicting selective pressures that vary on both temporal and spatial scales may lead to coexistence of both symbionts in anemones in the genus Anthopleura, constituting an xgument for multiple roles for symbiotic algae in hosts from different environments. Grazing by anemone predators may affect the distribution of svmbiotic algae in A. eleamtissima on local scales, and indirectly provides a mech&ism for the dispersal of zoochlorellae to anemone populations on larger scales. Freviously, only environmental factors such as temperature and light have been proposed to limit the distribution of zooxanthellae and zoochlorellae in Anthopleura (O Brien and Wyttenbach 1980; Secord 1995; Saunders and Muller-Parker 1997). Our work suggests that biotic interactions between the host, its algae, and anemone predators are also important. Symbiotic algae may play a larger role in benthic communities by influencing the outcome of predator-prey interactions involving their hosts. Shannon Point Marine Center Western Washington University 1900 Shannon Point Rd. Anacortes, Washington Gide Leon Augustine Muller-Parker I Corresponding author, also of Dept. Biology, Western Washington Univ. We thank R. T Paine, members of the U.S. Coast Guard, and the M&r& Tribal Nation for access to the research site on Tatoosh Island where the fish were collected. We also thank C. Pfister and G. Jensen for advice on collection and maintenance of the fishes, B. Bingham for assistance with statistical analyses, and D. &cord and B. Binghan for reviewing the manusaipt and providing helpful advice throughout the study. Two reviewers provided helpful cfitiques of the manuscript. We thank C. Hand for providing the initial mspiration for this study, and the National Science Foundation for providing support (OCE and USE ).

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