Prey Capture by the Sea Anemone Metridium Senile (L.): Effects of Body Size, Flow Regime, and Upstream Neighbors

Reference: Sol. Blrll. 192: 73-86. (February, 1997)

Prey Capture by the Sea Anemone Metridium senile (L.): Effects of Body Size, Flow Regime, and Upstream Neighbors

KENNETH R. N. ANTHONY* The Royul Swedish Academy ofSciences, Kristineberg Marine Research Station, Kristineberg 2130, S-450 34 Fiskebiickskil, Sweden

Abstract. The sea anemone Metridium senile is a Due to the nature of near-bottom hydrodynamics, how- quantitatively important passive suspension feeder in ever, flow exposure and body size are inseparable factors hard-bottom communities on the west coast of Sweden (Koehl, 1977a; Vogel, 1981). As suspension feeders grow and occurs in aggregations with different size distribu- taller they become exposed to faster currents within and tions. This study tests the hypothesis that different polyp beyond the substratum-associated boundary layer, and sizes have different optimal flow regimes maximizing consequently to both greater drag and higher flux of poten- prey capture. Results showed that prey capture by M. tial prey (Wainwright and Koehl, 1976; Vogel, 1981). The senile is a function of both flow regime and polyp size, height of a passive suspension feeder in a given flow habitat and different optimal flow regimes exist for different size is therefore likely to involve a trade-off between maximiz- classes. Large anemones had a maximum feeding effi- ing food availability and minimizing flow forces and phys- ciency at the slowest flow, medium-sized anemones at ical stress. In soft-bodied passive suspension feeders such as moderate flow, and small anemones at moderate- to sea anemones, limitations as to how tall an individual can high-flow regimes. Small anemones showed consistently grow in a high-flow environment may, in part, be governed higher feeding rates (per unit of biomass and area of ten- by the extent to which flow forces cause deformation of tacle crown) at all velocities above 10 cm s-’ and exhib- the feeding apparatus (Koehl, 1976, 1977a), reducing prey ited less flow-induced deformation of the tentacle crown, capture and thus energy for growth and reproduction (Seb- suggesting that small anemones are better at feeding in ens, 1979, 198 1, 1982; Lesser et al., 1994). Vertically ori- moderate- to high-flow habitats. Different vertical pro- ented passive suspension feeders of different sizes are there- jections of large and small anemones in the boundary fore likely to have different ranges of optimal flow velocities layer could only partly account for differences in feeding at which the physical stress is minimized and potential for success among size classes. Feeding rate was also a func- prey capture is maximized. Many sessile cnidarians are, tion of upstream conspecifics, declining asymptotically however, capable of polyp degrowth and indeterminate to 30% of the maximum rate. The negative effects of growth of the genet, in part through variable extents of neighbors on feeding in aggregations with clonal rather asexual proliferation such as pedal laceration (Buckhn, than polyp growth appear to be compensated for by the 1987; Anthony and Svane, 1995), polyp fission (Francis, generally higher feeding efficiency of small polyps. 1979; Sebens, 1980) and colony fission (McFadden, 1986). These capabilities result in size plasticity of the polyp (or Introduction colony) as well as of the clone. Small clones of large polyps Flow habitat and body size are both important factors in (or colonies) in low-flow habitats and large clones of small the feeding biology of benthic, passive suspension feeders. polyps (or colonies) in high-flow habitats constitute altema- tive solutions for maximizing prey capture and the positive energy balance of the genet. In the latter case, however, the Received I8 October 1995; accepted 25 October 1996. * Current address: James Cook University of North Queensland, De- extent to which the relationship between polyp size, flow, partment of Marine Biology, Townsville Qld. 48 1 1, Australia. and prey capture is modified by the presence of neighbor-

73 74 K. R.N. ANTHONY ing conspecifics (or clone members produced by asexual different optimal flow regimes that reflect the size distri- reproduction) has been demonstrated in only a few passive butions in natural populations. (octocorals: McFadden, 1986) and active (phoronids: The objectives of this study are to (1) quantify prey cap- Johnson, 1990; bryozoans: Okamura, 1992) suspension ture in M. senile at a range of polyp sizes and flow veloci- feeders. ties, (2) test whether combinations of polyp size and flow In this paper, the sea anemone Metridium senile is regime that maximize prey capture reflect size-frequency used for testing the effects of flow, polyp size, and up- distributions found in different flow habitats in situ, and stream neighbors on the feeding success of soft-bodied, (3) test whether prey capture in M. senile is, in part, a passive suspension feeders. Five features render M. senile function of the number of upstream conspecifics. a good model for such studies: (1) The projected area of the tentacle crown increases more-or-less isometrically Materials and Methods with body size (Sebens, 198 1); (2) new tentacles of a de- All experiments were conducted in a laboratory flume termined size are added to the tentacle crown as the (300-cm long, 47-cm wide, 18-20-cm water depth), de- anemone grows (Sebens, 1979) so that the spacing and signed as described by Vogel ( 198 1). A constant flow was size of filtering elements are the same for large and small ensured by controlling revolutions of the propeller by a anemones; (3) the size of prey (zooplankton) taken does Panasonic 501 inverter. Flow straighteners were not increase significantly with anemone size (Purcell, mounted at the entrance of the flume channel to reduce 1977; Sebens, 198 1; Sebens and Koehl, 1984); (4) it is turbulence to a level resembling near-bed field condi- capable of polyp degrowth (in part through asexual re- tions. Prey used in all experiments were newly hatched production by pedal laceration) and thus has an intrinsic nauplii of Artemia salina, which measure about 600 pm potential for adjusting its body size to the flow environ- in length and are within the mid-range of prey sizes re- ment; and finally (5) it often forms dense, clonal aggre- ported to be taken by M. senile in the field (Sebens and gations (Anthony and Svane, 1994) in which prey cap- Koehl, 1984). Artemia nauplii do not show the escape ture per polyp is likely to be influenced by the presence responses characteristic of some natural prey (Trager et of adjacent clonemates. al., 1994) so their use may produce overestimates of Metridium senile is a ubiquitous member of the hard- prey-capture rates in situ. That potential drawback was bottom community of most northern waters (Hoffmann, outweighed by the advantages that the non-evasive Ar- 1976; Fautin et al., 1989) and occurs in different size dis- temia nauplii are less likely to confound flow effects on tributions in different flow environments (Hoffmann, capture rates and can be reared in replicable batches. 1976, 1986; Shick et al., 1979; Shick and Hoffmann, 1980; Anthony and Svane, 1994). For example, in high- Flow measurements flow channels on the west coast of Sweden where the cur- Feeding experiments were carried out at six preset flow rent velocity frequently exceeds 100 cm s-l, the walls regimes: 4, 10, 17, 20, 28, and 44 cm s-‘, measured at and bottoms are carpeted by dense populations of small 10 cm above the flume floor by visually tracking and (2-3-cm-high) M. senile. Conversely, in low-flow habi- timing particles over a 25-cm trajectory within the work- tats where the current rarely exceeds 5 cm s-‘, large (20- ing section of the flume. To determine the local flow ve- 30-cm-high) M. senile predominate (Anthony and locity experienced by each anemone size class in a given Svane, 1994, 1995). In moderate-flow habitats, popula- flow regime, the vertical flow profile between 0.2 and 15 tions of M. senile are generally composed of intermedi- cm above the flume floor (l-cm intervals) was deter- ate-sized anemones (Shick, 199 1; and pers. obs.). Previ- mined from a matrix of 16 X 6 point samples taken ous studies have suggested that differences in size distri- within a plane normal to flow. These local flow velocities butions of M. senile can be attributed to the physical were measured with a thermistor probe (LaBarbera and effects of flow on the anemone body plan (Koehl, 1977a; Vogel, 1976) calibrated according to the method de- Shick and Hoffmann, 1980); genetic differences between scribed by Vogel ( 198 1, p. 3 16). The development of a local populations or clones (Shick et al., 1979; Shick and turbulent boundary layer was evident at all flow regimes, Dowse, 1985; Hoffmann, 1986; Anthony and Svane, and the local flow velocities measured at 0.2- 1 cm above 1994); and effects of substratum instability, which influ- the flume floor were generally 50% of those measured at ence the rate of laceration and thereby inversely affect a height of 10 cm ( UlO). The flow profiles obtained in the polyp and clone size (Anthony and Svane, 1995). Trade- flume at the six experimental flow regimes are depicted offs between polyp size and prey capture in different flow in Figure 1. regimes are likely to structure populations of this ecolog- ically and morphologically plastic species (Shick, 199 1). Distribution of nauplii in thejlume Nevertheless, no studies have experimentally tested the A comparison of the prey-capture successof different hypothesis that different polyp sizes of M. senile have size classesof passive suspension feeders requires the as- PREY CAPTURE BY SEA ANEMONES 75

0 5 10 15 20 25 30 35 40 45 50 Flow velocity (cm 8) Figure 1. Flow profile as a function of flow regime in the working section of the flume. Flow regime is referred to as the velocity measured at 10 cm above the flume floor (Z/,0). Error bars represent + 1 SE of 6 isobath measurements. sumption of a uniform and constant distribution of prey (y[,) tentacle tips) was determined for each group of items in the water column. Therefore, deviations from anemones during experiments. These values were used an even, vertical distribution of Artemia due to nauplii to compare vertical feeding zones and local flow veloci- swimming or hydrodynamic sorting were determined by ties experienced by different size classes and to calculate simultaneous sampling from 10 different heights above feeding efficiencies. Furthermore, the ratio of tentacle- the bottom in the working section of the flume. Samples crown surface area (s) to ash-free dry weight of individ- were collected with a comb of 4-mm acrylic pipes spaced ual polyps (AFDW) was used to indicate and compare 15 mm apart and pointing into the current, each pipe the degree of tentacle-crown deformation caused by flow connected to a silicone tube (see Muschenheim, 1987). forces. Ash-free dry weight was used as denominator One-liter samples were taken at each height, and sam- rather than a linear dimension because it provides the pling was replicated three times (l-h intervals) for every least variable measure of size. During each feeding cx- flow regime. The numbers of nauplii were standardized periment, tentacle-crown diameter (TCD, mean of two to a percentage distribution and tested using a replicated diameters taken at right angles to each other and de- G-test for goodness-of-fit (Sokal and Rohlf, 198 1). Sig- scribed by the outermost tentacle tips) for each anemone nificantly higher concentrations of nauplii were found was measured with callipers and used in calculating ten- close to the bottom of the flume channel at U10 = tacle-crown area (S = T(TCD/~)~). 4 cm s-’ (G,> = 55.4, P < 0.0001) and U10 = 10 cm SK’ (G,, = 20.1, P < 0.0 I), but the vertical distribution was Feeding experiments: sampling and experimental uniform at UjO = 17,20,28, and 44 cm s-’ (P > 0.05). design

Verticalfeeding zone and tentacle-crown deformation Three size classes of anemones within the full size range of M. senile were sampled in the Gullmarsfjord on The height range of the tentacle crown above the flume the west coast of Sweden, from three sites that experience floor (measured at the uppermost (JQ,) and lowermost different prevailing current regimes. Large anemones 76 K. R.N. ANTHONY

(6.0-6.5cm pedal disc diameter, pdd) were collected in ringe, and anemones were frozen and freeze-dried for the central Gullmarsfjord where the current is generally 48 h. After weighing, the dried anemones were com- low (~5 cm s-l), medium-sized anemones (2.5-3.0-cm busted for 12 h at 500°C and the ash-free dry weight pdd) were collected in a sound experiencing an interme- (AFDW) was obtained by subtracting ash weight from diate current regime (lo- 15 cm s-l), and small anemo- dry weight. nes (l-2 cm pdd) were sampled in a narrow channel where the current frequently exceeds 100 cm ss’ (see also Analysis ofif&ding experiments Anthony and Svane, 1994). In the laboratory, the anem- The natural logarithm of prey concentration was plot- ones were allowed to attach to panels (terracotta tiles ted with time, and the expected relationship measuring 10 by 20 cm, 3 mm thick) submerged in seawater tables. Excess anemones were removed from the Ln(C,) = -Ft + LnCo (1) panels so that a single row of 2-4 contiguous anemones was established on each panel. was fitted to the data using linear regression analysis and Prior to each experiment the flume was filled with fil- tested using Pearson’s product-moment correlation (So- tered (~20 pm) seawater freshly collected at 30-m depth kal and Rohlf, 198 1). The relationship is a linearization in the fjord (3 l-33%0 salinity and 8-l 1°C). The volume of the function c = c e-l”’ ofthe system when full (20-cm depth) was 400 + 2 1. Two 1 0 (2) panels with anemones attached were placed aligned on the bottom of the flume in the working section, so that a describing the exponential decrease in prey concentra- single row of 3-8 anemones was oriented perpendicular tion with time in a closed system (Leversee, 1976) where to flow. The anemones were allowed 12-24 h to accli- C, and C, are the concentrations of prey (nauplii 1-l) at mate to the selected flow regime and to fully expand be- the times t and to, respectively, and F is the clearance fore the feeding experiment was run. Immediately before rate (min-‘) of the suspension feeder. F depends on the an experiment, a standardized initial concentration (C,,) features of the feeding structures such as the size and of 150 f 20 Artev~ia nauplii 1-l was obtained by carrying density of tentacles per square centimeter of tentacle- out dilution series in 2000-ml beakers and calculating crown area (Sebens, 1981), orientation relative to flow batch concentrations and C,. This concentration was as- (Leversee, 1976; Johnson and Sebens, 1993), height sumed to be below that causing saturation of the anemo- above the substratum (Muschenheim, 1987), and prey nes, since only a small percentage (~5%) of the tentacles availability. The total clearance rate of the group of were occupied in prey capture at any given time. The anemones (F,,,) was the slope ofthe regression line +95% overall prey capture obtained in the experiments was CL, and the maximum feeding rate was determined as therefore assumed to be insignificantly affected by the C, F,,,Co V (nauplii min-‘), where V’is the water volume (1) chosen. of the system. To account for settlement and accumula- So that concentration of prey could be plotted as a tion of prey that could not be explained by anemone function of time, five 140-ml water samples were taken feeding, control experiments were conducted using simultaneously from the upstream section of the tank at anemone mimics. To be able to compare the retention of t = 0 and after every 10 min during the following 70- prey among anemone size classesin a given flow regime, 90 min. Because the total sampling volume was less than feeding rates were expressed basedon ash-free dry weight 3% of the system volume, sampling volume was not re- (AFDW) and square centimeter of tentacle-crown area placed or corrected for in the analysis. Samples were (S) at to. The empirical, maximum feeding rate per taken using a rack of fixed pipettes (2 mm thick and square centimeter of tentacle-crown area was thus deter- 20 cm long) arranged along a horizontal transect normal mined as to the direction of flow and connected by silicone tubes CoVF,,, - Fcmro,) Feeding rateMax,cm-2= (3) to a rack of syringes on the outside of the tank. Sampling S was done manually and isokinetically during 30 + 3 s to minimize variation due to prey patchiness. The samples and the maximum feeding rate per gram of ash-free dry were immediately filtered through a plankton mesh (60- weight was calculated as pm) to give 50-ml concentrated suspensions, and the CoVFtot - Fcontrd nauplii in each sample were counted directly using a dis- Feeding rateMax,AFDW-l= (4) AFDW secting microscope. The proportion of nauplii damaged by handling and by the flume propeller was less than 5%. Only the control experiment run at the lowest flow ve- To determine feeding relative to anemone biomass, the locity (4 cm s-l) produced a significant depletion rate anemones were dislodged from the panels 24 h after each (Fcontro,C,V f CL (nauplii min-‘) = 0.36 -t 0.18, P = experiment, any food boluses were removed with a sy- 0.02) and this was accordingly subtracted from feeding PREY CAPTURE BY SEA ANEMONES 77 experiments run at this flow speed. Feeding rates of sistent decline with increasing flow regime (Fig. 2). The different size classes at a given flow regime were com- feeding zone of large anemones was especially affected pared using an unplanned comparison (the Tukey- by flow-their mean height at the highest flow (Y’,,,~~”+ Kramer method; Sokal and Rohlf, 198 1). SE = 4.2 ? 0.2 cm) was only 50% of that recorded at Feeding efficiencies (E) are useful in comparing feed- the lowest flow regime (yMvleanf SE = 8.2 f 0.9 cm). A ing performance among size classes as well as in compar- pronounced downstream bending of anemone columns ing feeding performance of a size class among flow re- with increasing flow occurred (Fig. 2). The three size gimes, and were calculated as the number of prey items classes experienced different local flow velocities (U,,, es- captured relative to the number that would pass through timated from flow profiles in Fig. 1) in a given flow re- the space occupied by the feeding appendages ifthe latter gime because of their different positions in the boundary were not there (see Patterson, 199 1). The maximum layer. The uppermost tentacles of large anemones expe- number of prey items passing the projected feeding sur- rienced about twice the flow velocity of medium and face perpendicular to flow (Spr, cm2) per umt time is a small anemones, which were positioned deeper in the product of the concentration of prey at to(Co, nauplii ll’) turbulent boundary layer (Figs. 1 and 2). Differences in and the flow velocity (U,,, cm s-l) at the level of the feed- local flow speeds were less noticeable among medium ing structures (y), hence and small anemones. Tentacle-crown deformation, indicated by a decreas- 1 60 s NPassing= SI,prGlu~~ 1ooo cm3 X min (5) ing ratio of projected tentacle-crown area to ash-free dry weight (S/AFDW) with increasing flow, was most pro- S’,rr was calculated as an ellipsoid described by the height nounced for large anemones (Table I). The projected and width ranges of the tentacle crown (perpendicular to prey-capture surface of large anemones at U10 = the flow direction), from which the projected, transverse 44 cm s-’ was only one-third of that recorded at U10 = sectional area of the uppermost part of the column (the 4 cm s-‘. Tentacle-crown deformation of small and me- parapet; see Manuel, 1988) was subtracted. The feeding dium-sized anemones was noticeable only at flows be- efficiency (E) was then expressed as tween 4 and 17 cm s-‘. In that range they showed an initial increase in S/AFDW, presumably indicating incom- ,y - Nw-J - FV 16.7 cm3 1-l (6) plete tentacle-crown extension at the lowest flow Npassing S(/,lJJJ~ s min-’ velocity. Moreover, the generally lower S/AFDW ratios where Uncaptured= C, VF (nauplii min-I). of large relative to small anemones corroborates earlier findings (Sebens, 1981) that larger M. senile have a Eflect qfupstream neighbors smaller prey-capture surface per unit of biomass.

To determine the effect of upstream neighbors on the Feeding rates feeding rate per square centimeter oftentacle crown area, a series of experiments analogous to the above were con- Feeding rates of the three size classes of M. senile ducted using six patch sizes of anemones. Patch size was showed drastic changes with increasing flow, regardless expressed as the number of parallel rows of anemones of unit (per polyp, square centimeter of tentacle-crown aligned perpendicular to flow on the bottom of the area, or gram ofash-free dry weight, Fig. 3). Feeding rates flume. To exclude variation caused by flow and anem- tended to increase linearly and monotonically with flow one size, all experiments were conducted using anemo- over the range 4- 17 cm s-’ for all size classes, indicating nes within an intermediate size range (3-4-cm pdd), and that the availability of prey is a function of flow in low to run at the flow speed at which this size class had its max- moderate flow regimes. On a per-polyp basis, large imum feeding efficiency (see Results). Effect of upstream anemones captured 3- 10 times more nauplii than small neighbors on prey capture per square centimeter of ten- and medium-sized anemones within the flow range 4- tacle crown was tested using the Tukey-Kramer method 17 cm s-’ (Fig. 3A). Above 20 cm s-‘, however, the feed- (Sokal and Rohlf, 198 1). ing rate of large anemones declined rapidly with flow and converged with those of small and medium anemones, Results which remained constant above 20 cm s-‘. On a per-biomass basis, the pattern was partly reversed: small anem- Vertiral,feeding zone and tentacle-crown deformation ones showed 2-3 times higher feeding rates than me- The height of tentacle crowns above the flume floor dium-sized anemones, which in turn showed higher (y, from lowermost to uppermost tentacle tips), and thus feeding rates than large anemones, over the flow range vertical feeding zone, of large anemones was 2-3 times lo-44 cm s-’ (Fig. 3B). At the slowest flow, medium- that of medium and small anemones, and showed a con- sized anemones showed significantly lower feeding rates 78 K. R.N. ANTHONY

q Small, A Medium, + Large 15

0 10 20 30 40 Flow regime ( UIo, cm s-l )

Figure 2. Vertical feeding zone (range of tentacle-crown heights) of the three size classes of Mrlridi~~m senile as a function of flow regime. Error bars are f 1 SE of 3 to 9 anemones. The inset shows the typical posture ofa medium-sized anemone at moderate flow; the arrow indicates flow direction. Small anemones: 1 .O-2.0 cm in pedal disc diameter (pdd), medium: 2.5-3.0 cm pdd, and large: 6.0-6.5 cm pdd. than did both small and large anemones. Interestingly, crease in prey capture per unit biomass at Ulo > feeding rates based on feeding-surface area (S, Fig. 3C) 17 cm s-‘. and on anemone biomass displayed the same general patterns, perhaps reflecting isometric growth (Sebens, Fcwhg ~~~iiciencic.s 198 1). One noticeable difference among the sets of data The three size classes of M. senile demonstrated three is, however, that large anemones showed a significant de- distinct flow optima, inversely related to size class, at

Small ( I .O-2.0 cm pdd) Medium (2.5-3.0 cm pdd) Large (5.5-6.0 cm pdd)

UN) SJAFDW k AFDW + SE S/AFDW f AFDW + SE S/AFDW + AFDW* f SE (cm s ‘) n SE (cm* g-‘) (9) n SE (cm* g-‘) k) n SE (cm* 9-l) k)

4 9 64.99 + 6.24 0.156~0.019 7 43.86 f 2.44 0.635 + 0.048 3 56.31 + 7.14 2.827 2 0.403 10 6 84.09 * 3.18 0.148 + 0.009 5 49.52 f 3.31 0.682 f 0.052 3 53.67 f 7.48 2.827 k 0.403 17 8 52.48 f 3.99 0. I59 +- 0.022 5 40.86 f 3.3 1 0.663 f 0.058 3 43.39 f 3.92 2.827 f 0.403 20 8 47.80 -+ 2.83 0.160 iz 0.020 5 36.48 + I .92 0.650 -+ 0.06 1 3 29.61 f 3.17 2.827 f 0.403 28 7 47.80 f 3.6 I 0.101 kO.015 - - - 44 6 44.74 f 3.96 0.148 Ik 0.009 4 36.37 f I .09 0.541 kO.016 3 20.56 f 4.16 2.827 f 0.403

Size classes were based on measurement of pedal disc diameter (pdd). The degree of tentacle-crown deformation is quantified as the decrease in ratio of tentacle crown area (S) to ash-free dry weight (AFDW) with increasing flow (U,,). SE denotes standard error of n = 3 to 9 anemones. * The same three large anemones were exposed to all flow regimes. PREY CAPTURE BY SEA ANEMONES 79

800 tain up to 25.7 f 2.0% of the nauplii passing the pro- : .” jected area of the tentacle crown at their optimal flow E speed ( U10 = 20 cm s-l). The feeding efficiency of all size -a 600 3 classes decreased monotonically beyond their optimum. i? := At all flow velocities except the lowest one, small anem- z 2 400 ones were significantly (2-3 times) more efficient than z medium-sized anemones, which in turn were about B E twice as efficient as large anemones; these results are 200 2 analogous to the pattern of feeding rates based on bio- a 8 mass and area of feeding surface. Lk 0 Efect of upstream neighbors 1500 The feeding rate per unit area of tentacle crown of me- 7 dium-sized M. senile declined significantly with increas- .g 1200 ing numbers of conspecifics upstream (6.45 + 0.45 to : M 2.25 + 0.30 nauplii mini’ cmb2, both &95% CL) (Fig. 5). 2 900 The effect of upstream neighbors was most pronounced within small aggregations of anemones (2-4 rows). In- & 3 600 creasing the number of aligned rows of anemones from E 7 to 16 did not reduce the feeding rate per unit area of tentacle crown, and thus indicated a threshold at which the feeding rate per polyp was unaffected by the addition of upstream neighbors.

Discussion Feeding rates and eficiencies The combinations of polyp size and flow regime at which prey capture of Metridium senile is maximized are in good agreement with the pattern of population structures and flow habitats observed in the field, suggesting that size distributions of M. senile are, in part, based on the ability to utilize seston flux. Interestingly, small anemones were generally more efficient at retaining prey d than both medium and large anemones over the full flow 0 IO 20 30 40 range. Large anemones were, however, more than twice Flow regime (U,,, cm se’ ) as efficient as medium-sized anemones at the slowest flow, but this relationship was reversed at moderate to Figure 3. Feeding rates (nauplii min-‘) per (A) polyp, (B) gram of high flow. The generally higher feeding rate per unit area ash-free dry weight, and (C) unit area of tentacle crown of Mctridium smile as a function of body size and flow regime. Error bars are *95’% and per unit biomass of small anemones may allow rapid confidence limits. All comparisons among size classes are significant at growth to a size at which they can better compete for any given flow regime except at L/ r. = 4 cm s-‘. Groups with overlap- space, avoid size-selective predation (Harris, 1986), and ping error barsare not significantly different by the Tukey-Kramer test. reproduce sexually (Anthony and Svane, 1994), pro- Regressions for the determination of F were highly significant in all vided that the energy input is used in polyp growth rather experiments (P < 0.001, R > 0.88). than in clonal growth by pedal laceration (see below). The maximized feeding at a high flow speed of small M. senile is inconsistent with other studies on prey capture which the feeding efficiency (E> was maximized (Fig. 4). (e.g., Okamura, 1984, 1985; McFadden, 1986; Best, Large anemones showed a maximum feeding efficiency 1988; Leonard et al., 1988, Dai and Lin, 1993) and at the slowest flow (Ulo = 4 cm s-l), medium-sized growth (Okamura, 1992; Eckman and Duggins, 1993) of anemones at low to moderate flows (lo- 17 cm s-l), and tentaculate suspension feeders. In these studies maxi- small anemones at moderate to high flows (lo- mum rates of feeding, growth, or both were generally as- 20 cm s-l). Small anemones were able to capture and re- sociated with low flow speeds. A direct comparison 80 K. R.N. ANTHONY

20 30 Flow regime (U,, cm C*)

Figure 4. Feeding efficiency (number of nauplii captured per number of nauplii passing, see Eq. 5 and 6) as a function of flow regime in three size classes of Metriditrm senile. Error bars are ?95% confidence limits. All comparisons among size classes are significant at any given flow regime except between small and large anemones at l/r0 = 4 cm s-‘. G roups with overlapping error bars are not significantly different by the Tukey-Kramer test.

among studies of flow, body size, and prey capture is sons of size per se among different taxa of suspension difficult, however, because different ranges of size and feeders are complicated by differences in their structural flow regime are used in different studies. Also, compari- organization.

N= 102

I 5 10 15 Rows of anemones perpendicular to flow

Figure 5. Effects of upstream neighbors in Mefridium senile. Feeding rate (nauplii min-‘) per square centimeter of tentacle crown as a function of the number of upstream conspecifics. Error bars are ?95% confidence limits. Groups underlined at the same level are not significantly different by the Tukey-Kramer test. PREY CAPTURE BY SEA ANEMONES 81

The maximum prey-capture efficiency of M. senile effective in upstream capture (the circumference of ten- from the Gullmarsfjord (25.6 + 2.0%, small anemones) tacles facing upstream or perpendicular to flow) when is only half of that reported by Lesser et al. ( 1994) for M. the anemone is bent downstream relative to the total ten- senile from the Gulf of Maine (40% for offshore and 52% tacle crown area is likely to be greater for small anemo- for coastal anemones). Data on prey capture were, how- nes. Subtracting the projected area of the upper part of ever, not given in relation to flow speed although a sig- the column from the surface area of the tentacle crown nificant tentacle-crown deformation (50%) at increasing accounted to some extent for such geometric differences. flow was recorded, as also found in this study. The feed- However, size-related differences in the spacing of open- ing efficiencies determined for M. senile in this study are ings in the capitulum at the base ofthe tentacles were not also generally lower than those of the sea pen Ptilosarcus accounted for. If such differences exist, mainly as a result gurneyi (Best, 1988) which were up to 42%, decreasing of differential convolutions of the tentacle crown, they with flow to 30% within a narrow low-flow range (1.5- are likely to affect the size-specific feeding efficiencies (J. 5.0 cm so’), but are comparable with whole-colony effi- M. Shick, pers. corn.). ciencies of the octocoral Afcyonium siderium (Patterson, In moderate to high flow velocities, a great proportion 1991) in moderate flow regimes. However, the feeding of the tentacle crown of large anemones is hidden from efficiency of A. siderium is inversely related to both col- the upstream flux and is thus engaged in wake feeding, ony size and flow speed (Patterson, 199 l), whereas the which is likely to be less effective than upstream feeding relationship between feeding, size, and flow shows a (Shimeta and Jumars, 199 1). Small anemones may ben- more complex pattern in M. senile. These different pat- efit from both upstream and wake feeding at comparable terns may, in part, be due to the different filtering struc- flow rates, whereas wake feeding is likely to be the pre- tures and tentacular organizations between solitary and dominant mode of feeding for large anemones in mod- colonial anthozoans, and to differences in structural erate to high flow. However, due to the higher Reynolds flexibility. number associated with large animals (Shimeta and Ju- The increasing feeding rates as a function of ambient mars, 199 1), downstream vortex formation is more pro- flow within the low to moderate flow range corroborates nounced for large anemones. This effect may, in part, earlier assumptions that moderate-flow habitats provide be beneficial in providing a leeward region of enhanced higher seston availability than low-flow habitats (Shick retention efficiency through reduced flow velocities (Pat- and Hoffmann, 1980; Sebens, 1984; Shick, 1991). The terson, 1984). flow range at which food intake per polyp or per biomass Although the probability of prey encounter increases is maximized, however, is different between size classes. with flow, so does the risk of dislodgement of captured Large anemones showed a relatively distinct maximum prey, and an optimum local velocity must be within the at lo-17 cm s-l, whereas small and medium anemones range over which retention significantly exceeds dis- maintained a constant food intake above 10 cm SC’. lodgement of encountered prey. Both the capacity for re- These different responses to flow are likely to explain, in tention by and the risk of dislodgement from the tenta- part, the differences in size distribution of M. senile cles of sea anemones and of passive suspension feeders across flow habitats. In high-flow habitats M. senile typi- in general may vary among size classes and among geno- cally forms dense aggregations of small anemones mo- types. The small M. senile from high-flow habitats may nopolizing vast areas of rock wall and consisting of only be better adapted to feeding in a high-flow environment a few clones, whereas populations in low-flow habitats by being equipped with a more efficient cnidom for both often comprise large and usually more scattered individ- subduing and retaining intercepted prey. Effects of flow uals from numerous clones (Anthony and Svane, 1994). forces on dislodgement of intercepted prey in cnidarian Only at the slowest flow were large anemones able to suspension feeders are, however, poorly understood achieve feeding rates and feeding efficiencies comparable (Patterson, 1984; Shimeta and Jumars, 199 1). to those of small and medium-sized anemones. Large anemones had a significant feeding disadvantage relative Vertical.fkeding zone and tentacle-crown dqfbrmation to small and medium anemones at flows greater than 10 cm SC’, and displayed a per-biomass food intake only The prey availability can for some passive suspension one-eighth that of the small anemones in very high flow feeders be adjusted to a given flow regime by means of regimes. One explanation for this pattern is based on behavior or change of posture, for example by regulating differences in the geometry of the tentacle crown of large the height and orientation of the feeding appendages and small anemones. Although the tentacles of large and (ophiuroids: Warner and Woodley ( 1975); crinoids: Hol- small M. senile have comparable geometry and size (Seb- land et al. (1987) Leonard (1989); sea anemones: Rob- ens, 198 I), the relative size of the oral disc increases with bins and Shick (1980) this study; polychaetes: Muschen- body size. Therefore, the proportion of tentacle crown heim ( 1987) Shimeta and Jumars, ( 199 1)) or by vertical, 82 K. R.N. ANTHONY

oriented locomotion of the whole animal (Anthony and arians is largely governed by the thickness and character- Svane, 1995). Differences in prey capture among small, istics of the boundary layer surrounding the organism, medium, and large M. senile in this study could not be which in turn are functions of organism size and flow explained fully by different local flow velocities at differ- regime (Patterson, 1992a). For example, Patterson and ent heights in the boundary layer. In fact, the local flow Sebens (1989) found that the rate of respiration in large velocities experienced at the mean level of the tentacle specimens of Metridium doubled over the flow range 7- crown of the three size classes in low to moderate flow 15 cm so’ due to the effect of water motion. A useful regimes did not differ by more than l-2 cm s-‘. Con- method for comparing metabolic cost across flow re- trasting local flow velocities due to differences in vertical gimes as well as size classes is the relationship between position were found only between large and small or me- Sherwood number and Reynolds number (Patterson and dium-sized anemones at the highest flow regime (6- Sebens, 1989; Patterson, 1992a, b). Sherwood number 8 cm s-l). A higher degree of downstream bending of (Sh) is a dimensionless index of metabolism, defined as medium-sized and especially large anemones due to pro- the ratio of mass flux per unit surface area assisted by portionately greater drag (Koehl, 1977a) explains the convection (F,,,,, p cm-’ h-‘) to that which would occur overlapping, vertical feeding zones of different size if diffusion through a stagnant layer of water was the only classes. Flow forces thus act in moving the feeding appa- mechanism of gas exchange. Reynolds number (Re) is ratus of large anemones into the boundary layer and the ratio of inertial to viscous forces acting on the flowing away from the maximum exposure, enabling some, water, and is an index of the strength of flow experienced though reduced, prey capture at even the highest ambi- by the organism. For Metridium, the functional relation- ent flow. ship between Sh and Re is Sh = 0.28 Re’.04 as found by Tentacle-crown deformation, and thereby a reduced Patterson and Sebens (1989). Since Re is a function of prey-capture area normal to flow, could to some extent body size and flow [Re = U, X TCD/v, where U,, is local account for the significantly lower feeding success of flow speed (cm so’), TCD is tentacle-crown diameter large anemones in regimes of moderate to high flow. (cm), and v is the kinematic viscosity of seawater ( 1.04 X Prey-capture surface per unit biomass decreased by more lop2 cm2 s-l)], Sh can be readily obtained for all combi- than 50% when altering the flow regime from 4 to nations of flow regime and size class in this study. Ex- 44 cm s-‘, affecting the volume of water filtered and the pected (flow-assisted) metabolic cost can be derived from rate of potential prey encounter accordingly, and proba- Sh as the convective mass flux (F,,,,, the numerator of bly also the spacing between tentacles (see also Lesser et Sh), normalized to biomass by multiplying with the ratio al., 1994). Best ( 1988) also found that the deformability of surface area to biomass (SA/AFDW, cm2 g-l), where of the sea pen Ptilosarcus gurneyi strongly affected fil- SA is the sum of tentacle surface area [see regressions in tration efficiency and volume of water filtered. The Sebens (198 l)] and surface area of the column. Accord- effectiveness of the feeding apparatus of a large, soft-bod- ing to Patterson ( 1992b) convective mass flux can be cal- ied suspension feeder is intrinsically apt to be more con- culated as F,,,, = Sh X D(C) - C,)/TCD, where D is the strained by flow forces than is that of a small suspension diffusion coefficient for oxygen (7.2 X 10m2cm2 h-l), C, feeder, because large animals are subject to proportion- is the oxygen concentration in the surrounding water ately greater drag (Koehl, 1977a) and shear stresses (x7 mg ll’), and Cj is the oxygen concentration at the (Koehl, 1977b) than are small animals in similar flow site of metabolism. For azooxanthellate cnidarians, C, conditions. Since the potential prey capture of, for exam- can be regarded as negligible (pers. corn., Mark Patter- ple, a sea anemone is a function of the surface area of the son). Expected metabolic rate per unit biomass (R,,, = feeding apparatus (Sebens, 198 I), the S/AFDW ratio is Sh X D X C, X SA/[TCD X AFDW], pg (g dry wt))’ h-‘) likely to be a useful indicator of flow-habitat suitability. as a function of flow regime for the three size classes of M. senile is shown in Figure 6. Feeding rates vs. metabolic cost Expected metabolic rate for all size classes increases as a linear function of flow regime, with a IO-fold increase To determine flow optima of passive suspension feed- in metabolic rate between lowest and highest flow speeds. ers, information on both energy intake and metabolic In accordance with allometric studies (e.g., Sebens, cost is necessary for every flow regime (Sebens, 1979, 198 I), metabolic rate is greater for small and medium- 1982). Although the pattern of feeding rates per unit of sized compared to large anemones, by a factor of about biomass suggests that small anemones generally have a y2. Interestingly, expected metabolic rate is higher for greater energy surplus than large and medium-sized medium-sized compared to small anemones at flow re- anemones regardless of flow regime, energy demand is gimes greater than 10 cm s-‘, probably due to the higher likely to vary among size classes as well as among flow local flow speeds (and hence Sh) experienced by me- regimes. Gas exchange, and thus metabolic cost, in cnid- dium-sized anemones (Figs. 1 and 2). Although energy PREY CAPTURE BY SEA ANEMONES 83

+ Small * Medium + Large

0 10 20 30 40 Flow regime ( UIo, cm s-’ )

Figure 6. Expected metabolic rate as a function of flow regime for the three size classes of Mefridium senile, based on mean Reynolds numbers for the study anemones and empirical mass-transfer relations from Patterson and Sebens ( 1989). See text for calculations. balance also depends on local food availability, food with flow. The flow optimum of medium-sized anemo- quality, and absorption efficiency (e.g., Zamer, 1986) nes, on the other hand, is likely to be located in the range the patterns of potential food intake (feeding rate) and 1 O-20 cm SC’, as their feeding rate is minimal at 4 cm s-’ expected metabolic cost provide a basis for relative com- ( ‘/3 of large and small anemones) and their expected met- parisons of potential flow optima among size classes. The abolic cost increases with flow at a relatively higher rate flow speed at which energetic cost counterbalances food than for the two other size classes. intake will be highest for the small anemones, intermedi- Use of mass-transfer theory to compare metabolic cost ate for medium-sized anemones, and lowest for large between individual M. senile in different flow regimes anemones. Due to very high feeding rates, small anemo- does not, however, take into account the differences in nes are able to maintain a more positive energy balance spatial distributions between large and small anemones. than both medium and large anemones at all flow speeds Large anemones are often widely separated from one an- 2 10 cm SC’. The almost IO-fold increase in feeding rate other, whereas small anemones (due to their pronounced of small anemones in the flow range 4-10 cm s-’ amply clonality) form dense patches structurally resembling exceeds the concomitant increase in metabolic cost over coral colonies (Anthony and Svane, 1994). Flow around this flow interval, and is likely to allow rapid growth of individual polyps in such patches is likely to be further juvenile anemones and lacerates in low-to-moderate reduced, resulting in a thicker diffusive boundary layer flow regimes. At higher flow speeds, however, feeding and a lower gas exchange than for small, spatially iso- rate remains constant, whereas metabolic rate increases lated individuals in similar flow habitats (see also Patter- linearly with flow. If the feeding rate of small anemones son and Sebens, 1989). at 4 cm SC’ is sufficient to meet basic energy demands, so is the feeding rate at 44 cm s-’ because both feeding rate Effects ofjlow andfeeding on reproductive patterns and metabolic cost increase IO-fold between lowest and highest flow. At the lowest flow speed, however, large One way in which M. senile might maintain an ener- anemones are likely to have a more positive energy bal- getically optimal polyp size in the prevailing current re- ance than the smaller size classes, given the comparable gime is by altering the rate of pedal laceration. Lacera- feeding rates of small and large anemones but the lower tion is a loss of tissue to the individual polyp (facilitating mass-specific metabolic cost of large anemones. Since degrowth), but also an effective means of clonal growth, large anemones only showed low weight-specific feeding so differential rates of laceration between local popula- rates without a convincing maximum, any energetic op- tions may have consequences for their size distributions. timum of this size class must be confined to low-flow re- The generally higher rates of laceration in populations of gimes because of the rapid increase in metabolic rate small M. senile from high-flow habitats relative to popu- 84 K. R.N. ANTHONY lations of large anemones from low-flow habitats support responsible for reduced downstream concentrations, and this hypothesis (Shick and Hoffmann, 1980; Anthony thereby, in part, account for the asymptotic rather than and Svane, 1994). Since large anemones cannot main- linear reduction in retention with increasing number of tain a positive energy balance in high-flow habitats, upstream neighbors (see also Frkchette et al., 1989). Fur- whereas small anemones can, any excess energy acquired thermore, gravitational deposition is likely to be more by high-flow anemones is likely to be allocated to clonal important in dense clones than in populations of scat- growth (through pedal laceration) rather than to polyp tered individuals on horizontal substrata, providing a growth. Laceration is also stimulated by feeding “rain” of seston that is independent of the number of (Bucklin, 1987), suggesting that asexual reproduction is upstream neighbors. Overall, these results suggest that one pathway by which energy surplus is translated into a increased clonal growth of M. senile in high-flow habitats greater genet biomass. Effects of feeding and ambient at the expense of polyp growth (see review by Shick, flow on laceration are, however, apt to be closely linked 199 1) may negatively affect net prey capture by the genet due to the direct proportionality between flow and seston through feeding interaction between clonemates. Con- flux, and hence potential particle encounter. By obtain- versely, predominant polyp growth and reduced clonal ing an optimal polyp size in a given flow habitat through growth in low-flow habitats is likely to enhance prey cap- growth or degrowth (via laceration), the energy available ture by excluding the effect of neighbors. The generally for clonal growth, sexual reproduction, and hence genet higher feeding efficiency of small polyps of A4. senile fitness can be further enhanced. Clonal growth as op- may, however, compensate for the negative effects of posed to polyp growth in high-flow habitats creates the neighbors in dense, clonal aggregations if the prevailing energetic potential for the genet to grow indefinitely flow conditions provide a correspondingly higher flux of without size-energy constraints, because the addition of prey. new polyps to the clone increases feeding surface and energetic cost linearly (Sebens, 1979). Conversely, growth Acknowledgments to a maximum polyp size in low-flow habitats enables I thank the administration and staff of Kristineberg maximum feeding and thus energy input (this study), Marine Research Station for providing laboratory facili- and also a maximum per-biomass reproductive output ties and technical assistance. Thanks are especially due (Anthony and Svane, 1994). to Ken Sebens for reviewing the penultimate draft, and to Terry Hughes, Bette Willis, The Coral Discussion .F&zt cfupstream neighbors Group at James Cook University, Henrik Glenner, Pia Considering the clonal nature and high polyp densities Anthony, and Robert George for valuable discussions of most populations of M. senile, the presence of up- and comments on earlier versions of the manuscript. I stream neighbors is likely to be an important factor am grateful to Mark Patterson for his advice on calcula- affecting the energy input of both the polyp and the tions of expected metabolic cost. Malcolm Shick, Wil- clone. Furthermore, the effect of upstream neighbors on liam Zamer, and Barbara Best improved the final manu- near-bed prey availability downstream may select for script. Thanks are also due to Walt Doyle for assistance large size in some flow habitats, despite a relatively in the laboratory. This work was supported by the Nor- dic Council for Marine Biology, Nordic Academy for greater food intake in small anemones, and thereby con- Advanced Studies, the Axe1 Hemmingsen Grant, and the tribute to structuring local populations. The asymptotic Hierta-Retzius Foundation (Royal Swedish Academy of relationship between feeding rate per unit area of tenta- Sciences). cle crown and number of upstream conspecifics, on the other hand, indicated that the potential feeding capacity was not reduced to below about 30% of the situation Literature Cited without neighbors upstream. A likely explanation for Anthony, K. R. N., and I. Svane. 1994. Effects of flow-habitat on this threshold is that individual anemones function as body size and reproductive patterns in the sea anemone Metridium roughness elements, increasing turbulence and eddy senile (L.) in the Gullmarstjord, Sweden. Mur. Ed. Prog. Ser. 113: 257-269. diffusivity downstream (Denny, 1988), thereby reducing Anthony, K. R. 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