physiological energetics of the intertidal sea anemone anthopleura elegantissima

Marine Biology 92, 299-314 (1986) Marine ===~

�9 Springer-Verlag 1986

Physiological energetics of the intertidal sea anemone Anthopleura elegantissima I. Prey capture, absorption efficiency and growth

W. E. Zamer *

Department of Zoology, University of Maine at Orono; Orono, Maine 04469, USA

Abstract

High-intertidal (H) individuals of the sea anemone Antho- pleura elegantissima (Brandt) are exposed aerially up to 18 h each day, unlike low-intertidal (L) individuals which may be continuously immersed over many days. Thus, H anemones experience shorter feeding periods compared to L anemones. From 1980 to 1982, H and L anemones were observed and collected at the mouth of Bodega Harbor in North Central California (USA) to determine whether any physiological adaptations mitigate the energetic effects of reduced feeding time in H anemones. Weight of prey in coelenterons of H anemones was three times more than that of L anemones following a single immersion period. This difference is not due to slower digestion rates in H anemones. Prey residence time in coelenterons (4 h) was equivalent in both groups. Different prey weights imply that ingestion rates were greater in H individuals. How- ever, all anemones had similar weight-specific feeding- surface areas. Different prey-capture rates result from increased receptivity to prey in H anemones, rather than from increases in feeding surface. Absorption efficiency was inversely related to ration size in anemones from both shore positions. H individuals absorbed food more ef- ficiently than L individuals fed equivalent rations. Ration, not exposure conditions, affected absorption efficiency. Daily growth rates were 1.5 to 1.8% and 1.2 to 1.4% of dry body weight in H and L anemones fed large rations (4.0 to 5.6% of dry body weight), respectively. H anemones fed smaller daily rations, approximating amounts of zooplankton captured naturally (1% of anemone dry weight), had higher growth rates and growth efficiencies than L anemones, which lost mass. Higher growth rates in H anemones, which are supported by higher prey-capture rates, result in attainment of minimum body size for reproduction in a relatively short period of time despite

* Present address: Department of Zoology, Iowa State University, Ames, Iowa 50011, USA

reduction in time available for feeding, thus improving relative fitness of these anemones in the upper intertidal zone.

Introduction

An important consequence of aerial exposure in intertidal invertebrates is a progressive decrease in time available for feeding as animal distributions extend farther into the upper intertidal zone. Intertidal invertebrates may reduce energy expenditures, increase rates of energy acquisition or both in response to the energy short-fall (Newell, 1979, 1980). Temperature changes arising from aerial exposure affect animal energetics (e.g. adjustments in rates of filtration and oxygen uptake in oysters: Newell etal., 1977; Buxton etaI., 1981), and interspecific variation can be correlated with intertidal distributions (e.g. rates of oxygen uptake in chitons: Murdoch and Shumway, 1980; energy budgets in limpets: Branch and Newell, 1978). However, few studies have focused on reduction in feeding time per se in a single species (see Griffiths and Buffen- stein, 1981). The integrated studies on the blue mussel Mytilus edulis which have partitioned the effects of temperature, exposure and food level on components of energy balance are important exceptions (Thompson and Bayne, 1974; Bayne and Widdows, 1978; Widdows and Shick, 1985).

Adaptations in passive suspension-feeders have re- ceived less attention than those of actively filtering bivalves. Shick (1981) demonstrated lower rates of energy expenditure in high-intertidal individuals of the sea anemone Anthopleura elegantissima relative to low-intertidal individuals. However comparisons have not been made of rates of prey capture in high- and low-intertidal individuals of passive suspension-feeders. One might expect an increase in prey-capture surface-area in compensation for reduction in feeding time in high-intertidal animals

300 W.E. Zamer: Physiological energetics ofAnthopleura elegantissima. I.

such as sea anemones. Such adaptations might reflect changes in other components of the energy budget (e.g. growth) between high- and low-intertidal individuals.

The symbiotic sea anemone Anthopleura elegantissima (Brandt) is an appropriate species to test these hypotheses. It is a spatially dominant inhabitant of the rocky intertidal zone of the west coast of North America, spanning a vertical range from mean lower low-water to approximately +2 m above tidal datum (Hand, 1955). The anemone may be exposed approximately 90% of the time in the upper intertidal (Ricketts, 1978) or not at all in the lower intertidal, and thus experiences variations in feeding time. Studies specifically examining adaptations to tidal position (see Shick and Dykens, 1984; Sebens, 1981b, 1982b, c, 1983) have not considered absorption efficiency or growth efficiency, which might change with feeding time.

This work reports field measurements of prey capture in high- and low-intertidal individuals of Anthopleura elegantissima. Values for absorption efficiency and net growth efficiency also were determined in anemones acclimatized to different experimental combinations of ration and physical tidal regime in order to assess the relative importance of these two factors on the biology of this species.

Materials and methods

Collection and maintenance of anemones

All individuals ofAnthopleura elegantissima (Brandt) were collected from the south jetty at the entrance to Bodega Harbor (38~ 123~ in north-central California, from summer 1980 to summer 1982. Generally, low- intertidal (L) anemones were collected at mean lower low- water, and high-intertidal (H) anemones were collected approximately 1.3 m above this unless otherwise stated. Differences in emersion time between H and L anemones have been illustrated previously (Fig. 1 in Shick and Dykens, 1984). Daily exposure of H and L anemones averages 15 to 17 h and 2 to 4 h, respectively (Ricketts and Calvin, 1968). The distribution of high-intertidal individuals at Bodega Harbor probably does not extend beyond 1.8 m above tidal datum, where anemones are extremely small. Some anemones were studied in Or0no, Maine, and these were shipped by air freight, and maintained at 15 ~ on a 12 h light:12 h dark photoperiod in filtered, recirculating seawater (33%0 S). Anemones used in Cali- fornia were kept in seawater tables inside the laboratory or in outdoor tanks containing circulating seawater. Anemo- nes in all experiments were cleaned of adhering debris.

Prey capture and prey-capture surface-areas

A static measure of prey-capture by Anthopleura elegantissima in the field was made at Bodega Harbor in June 1982 by sequentially collecting similarly sized H and L

anemones as they became exposed to air on two ebbing tides. High-intertidal anemones from two clones were collected 1.5 m above mean lower low-water; low-intertidal anemones from two clones were collected 1 m above mean lower low-water. Ninety minutes elapsed between the first aerial exposures of H and L anemones. Basal disc diameters of attached anemones were measured to the nearest millimeter; anemones were gently removed from the substratum and immediately immersed in and injected with 7% buffered (sodium cacodylate) formalin in seawater. Later, prey were removed from the coelenterons as described by Sebens (1981a), cleaned of adhering mucus, rinsed in distilled, deionized water and dried at 56~ to constant weight. Dry weights of prey were adjusted to compensate for weight loss during preservation (Omori, 1978). Basal disc diameters were converted to mass using separate regression equations for H and L anemones which related basal disc diameter to whole anemone reduced weight (i.e., weight in sea-water; Mus- catine, 1961; Sebens, 1981 a, 1982 a) and reduced weight to dry weight (60 ~

Prey-capture surface-areas were calculated from measurements taken from photographs of the oral surface of H and L anemones from five and four clones, respectively. Anemones shipped to Orono in May 1982 were individually placed in fingerbowls of seawater (15 ~ and allowed to attach. Other anemones were collected at Bodega Harbor in June, 1982 and allowed to attach to the bottom of seawater tables (12~ Basal disc diameters were then measured directly and converted to body mass as explained in previous paragraph. Average length and average diameter at mid-length of the tentacles (Fig. 1 A) and the formula for the surface area of a cylinder were used to calculate average tentacle surface-area (Sebens, 1981 a). Total tentacle surface-area (Fig. 1 C) is the average tentacle surface-area times the number of tentacles. Pro- jected surface of the tentacle crown (i.e., the circle described by the tentacle tips) and oral disc surface-area (Fig. 1 B) were calculated as areas of circles using the respective diameters. Projected tentacle surface-area was calculated as tentacle-crown surface-area minus oral disc surface-area. Total prey-capture surface-area (Fig. 1 D) is the sum of oral disc and total tentacle surface-areas.

Absorption efficiencies

Experiments in Orono were conducted on H and L anemones of similar mass collected in July, 1980 which had been acclimatized in a tidal simulator (Thompson, 1968) for 6 to 8 wk prior to measurement of absorption efficiency. Three clones each of H and L anemones were maintained either intertidally (I) (two 6 h emersion periods daily) or subtidally (S). Thus, four treatment groups (HI, HS, LI, LS) were maintained to distinguish the effects or~ absorption efficiency of acclimatization to particular tidal conditions (I or S) from those of original intertidal position at Bodega Harbor (H or L). The design accentuates

W. E. Zamer: Physiological energetics ofA nthopleura elegantissima. I. 301

ORAL DISC .~ DIAMETER

TENTACLEER

BASAL DISC DIAMETER s

B

D

Fig. 1. Anthopleura elegantissima. Surface-area measurements. (A) Linear measurements from photographs (basal disc diameter measured directly; (B) oral disc-surface area; (C) total tentacle-surface area; (D) total prey-capture surface-area

differences in feeding time while providing two low tides daily. Intertidally-maintained anemones experienced an irradiance of 30 to l l 0 / ~ E m -2 s -1 during air exposure (15 ~ to 18 ~ Subtidalty-held anemones were exposed to less than 30 ktE m -2 s -1 because of their immersion and greater distance from the light source. Anemones were fed freshly-hatched Artemiasp. nauplii (San Francisco Bay brand) adlibitum. The concentration of nauplii ranged daily from 55 to 1 040 per liter. Nauplii were continuously available to the anemones.

At the end of this acclimatization period, reduced weights were determined for several HS and LI anemones which were then dried (56 ~ 96 h) and weighed. These data were pooled and the resulting regression of dry vs reduced weight was used to convert reduced weights measured on all anemones removed from the simulator. Anemones were transferred individually to fingerbowls and maintained under the same tidal conditions except that all anemones experienced an irradiance of 100ktE m -2 s -1 continuously during the 12 h light period, and air temperature was maintained at 15 ~ Intertidally-maintained anemones (HI and LI) were given a single daily ration of adult Arternia sp., the calculated dry weight of which (see below) was 4.0% of dry weights of individual anemones. Subtidal individuals were given larger rations (5.6%) in proportion to their available time for feeding and concentration ofnauplii in the tidal simulator.

After absorption efficiencies were obtained under these conditions, an experiment was performed on the same anemones to distinguish the effects of ration and physical tidal regime on absorption efficiency. One half of the anemones in each of the four treatment groups were

acutely transferred to the alternate tidal condition but without the appropriate change in ration. For example, some HI individuals were switched to subtidal conditions but still were given an intertidal ration. Any change in absorption efficiency relative to control groups (those anemones not acutely transferred) was therefore due to the change in tidal regime and not to a change in ration.

Experiments at Bodega Harbor were conducted on two clones each of freshly collected H and L anemones. Anemones were maintained under natural sunlight and temperature conditions (water: 11 ~ to 13~ air: 13 ~ to 19 ~ in individual containers submerged in tanks with circulating seawater. High-intertidal anemones were kept intertidally as described above (HI) and L anemones were kept subtidally (LS). All anemones were fed rations of frozen adult Artemia sp. equivalent to 1% of anemone dry body weight. Dry weights were calculated from reduced weights as before, using regressions for fresh H and L anemones from the experimental clones.

Weights of rations for each individual were calculated from a regression of dry vs blotted wet weight of Artemia sp. and from the calculated dry weight (from reduced weight) of each anemone. Absorption efficiencies were obtained daily from those anemones which ingested all of the ration. Egesta were collected daily before each new feeding, rinsed in distilled water to remove salt, dried at 60~ for 72h, and weighed to the nearest 0.01 mg. Rinsing the egesta undoubtedly removed some dissolved organic compounds, but removal of particulates was pre- vented. Egesta of this species are coated thinly with mucus, most of which was probably not removed by rinsing. Loss of dissolved organics leads to slight over- estimates of absorption efficiency, and inclusion of mucus in egesta leads to slight underestimates. However, all egesta samples were handled similarly, so that relative differences in absorption efficiency accurately reflect the effects of treatment variables. Gravimetric absorption efficiencies (A g) were calculated as

grams ingested - grams egested Ag - grams ingested x 100%.

Absorption efficiencies for organic mass, and total carbon and nitrogen (Ao, Ac and An, respectively) were calculated using the general equation

f X r - f X e ( 1 -Ag) A x - x 100%, (1)

fXr

where organic, carbon and nitrogen mass fractions in dried samples of Arternia sp. (ration) and egesta were sub- stituted for f X r and fXe, respectively. Decimal fractions were used for Ag. Organic content of food, whole-body tissues and egesta was obtained by combusting samples at 550 ~ for 6 h. Carbon and nitrogen mass fractions were obtained from CHN analysis (see below - "CHN analysis"):

Energy content of the organic fractions [kJ (g organic wt) -1] of food (Er) and egesta (E~) was calculated using

302 W.E. Zamer: Physiological energetics ofA n thopleura elegantissima. I.

the results of CHN analysis (Gnaiger and Bitterlich, 1984). Energetic absorption efficiencies were then calculated as

Er(l - ash,.) - Ee[(1 -Ag) - ashe(1 -Ag)] Ae = x 100%, (2)

Er(1 - ashr)

where ash r and ashe are mass fractions of ash in food and egesta, respectively.

Digestion rates

Throughput time (Sibly, 1981), the interval between ingestion and first appearance of egesta, and the longest residence time of prey in the coelenterons were measured on anemones used in the absorption efficiency experiment at Bodega Harbor. Individuals were observed at 20 min intervals following ingestion of the daily ration on one day, and throughput time was noted. Time when egestion stopped in all anemones was taken as longest residence time of prey.

Energetic net-growth efficiencies were calculated from the energy contents [kJ (g organic mass) -1] of anemone tissues, ingested rations and egesta using CHN analysis (see below) and the following equation:

Ete [ We - - ashte (We) ] - Etb [ Wb -- ashtb (Wb) ] K2 = x 100%.

E~[R - ash~(R)l - E f [ F - ashf(F)] (3)

Wb and We are the dry weights of the anemones at the beginning and end of the experiment. Energy content of anemone tissues at the beginning of the experiments (Etb) was determined using separate anemones removed from the tidal simulator (Orono experiment) and freshly collected anemones from Bodega Harbor. Ere is energy content of anemone tissues at the end of the experiments. Mass fractions of ash in anemone tissues are similarly designated. R and F are dry weights of ingested ration and egesta, respectively; Er and E f are their respective energy contents; mass fractions of ash in ration and egesta are similarly designated.

Net growth efficiencies

Gravimetric net growth efficiency, K2 [grams growth (g absorbed ration)-lx 100%], was computed for the same experimental series of anemones in which absorption efficiencies were measured. In the Orono experiments, initial dry weight of the anemones was that calculated from reduced weight at the end of tidal simulation. At the end of the feeding experiment reduced weights were again measured and converted to final dry weights using the same regression. The difference between initial and final dry weights is the dry weight growth. Total wet weight of Artemiasp. ingested was converted to dry weight as described earlier, and from this value total measured dry weight of the egesta was subtracted to obtain the absorbed dry ration.

A separate series of control anemones in the same four treatment groups was used to check for changes in the relationship between reduced and dry weight, i.e., for changes in specific gravity. Individuals were weighed in seawater and then in distilled water before and after the feeding experiment, and ratios of seawater to distilled water reduced-weights were compared (Sebens, 1980). Changes in specific gravity following the feeding experiment indicate changes in ratios of the major biochemical constituents and, therefore, changes in weight-specific energy content of the tissues.

Gravimetric/s was computed in the same way for the Bodega Harbor experimental anemones, except that the separate regressions of dry vs reduced weight used in the absorption efficiency calculations were also used to calculate initial dry weight. Final dry weight was calculated from similar regressions using final reduced and dry (60 ~ 48 h) weights of the experimental individuals.

CHN analysis

Carbon, hydrogen and nitrogen (CHN) elemental analysis was used to calculate proximate biochemical composition and energy content of food, body tissues and egesta according to the methods of Gnaiger and Bitterlich (1984). Triplicate samples (0.6 to 7.5 rag) of oven-dried or freeze- dried anemone tissues and frozen adult Artemia sp. (San Francisco Bay brand), and of oven-dried egesta, were combusted (1 025~ and analyzed in a Carlo Erba elemental analyzer (Model 1106). Cyclohexanone-2,4-dini- trophenylhydrozone was the standard. Protection of dried samples from contamination with atmospheric water va- por was rigidly controlled. Any negative values for biochemical constituents were set to zero and the remaining constituent fractions were recalculated from the funda- mental stoichiometric equation [Eq. (2) in Gnaiger and Bitterlich (1984) as recommended by these authors].

Statistical analyses

All statistical analyses were performed using the Statistical Analysis System of programs (SAS, Cary, North Carolina, USA) unless otherwise stated. Angular transformations (Sokal and Rohlf, 1969) were used on all percentage data. Confidence limits of transformed means have been re- transformed to percent values and are therefore asym- metrical (Sokal and Rohlf, 1969). Although morphometric data are appropriately expressed as correlations, comparisons of linear relationships can be made only by covariance analysis. Hence, these data were expressed using regressions.


Table 1. Anthopleura elegantissima. Coelenteron contents of high- and low-intertidal anemones collected and preserved following one immersion period at Bodega Harbor. Basal disc diameters and prey weights are means (+ SD); dry body weights were calculated from equations in Fig. 4; prey-capture-surface areas were calculated from regressions in Table 2

Tidal Mean basal Dry body wt Mean dry wt N Prey-capture state disc diam (cm) (rag) of prey (mg) a surface/dry body

( _+ SD) ( _+ SD) wt (era 2 g ~)

High 1.7 (+0.2) 244.62 1.48 (+ 1.29)

Low 1.7 (_+0.3) 342.32 0.46 (_+0.34) P < 0.05

6 68.5

7 64.3

Values are means of measured dry weights multiplied by 2.0 to correct for weight loss in formalin (Omori, 1978). Means are correlated with the standard deviations. Probability value is from a Student's t-test for unequal variances using log-transformed variates (Sokal and Rohlf, 1969)

Table 2. Anthopleura elegantissima. Analysis of covariance (ANCOVA) of the square roots of surface areas (v; cm) vs basal disc diameter (x; cm) for high- and low-intertidal anemones. All slope comparisons were not significant and pooled slopes are shown. The square-root transformations yield nor- mally distributed variates

Surface area Tidal Linear equation N R 2 ANCOVA Probability state slopes intercepts

Oral disc H and L y=0.474 x+ 1.034 41 0.342 0.181 0.051

Projected tentacle H and L y = 1.720 x - 0.874 39 0.791 0.375 0.100

Tentacle crown H y = 1.706 x - 0.286 22 0.857 \ 0.801 0.023 L y = 1.706 x+ 0.064 20 0.830 J Total tentacle H y=2.276 x - 0.096 24 0.754 0.333 0.042 L y=2.276 x+0.360 20 0.891 1 Total prey-capture H y = 2.273 x + 0.232 22 0.821

0.527 0.003 surface-area L y=2.273 x+0.823 19 0.856 ]

Results

Prey capture and prey-capture surface-areas

Mean basal disc diameters of H and L individuals of Anthopleura elegantissima collected for coelenteron-content analysis were the same, 1.7 cm (Table 1). Dry weight of prey in the coelenterons of H anemones averaged more than three times the weight of prey found in L anemones (P < 0.05).

Mean basal disc diameters of H (2.1cm) and L (2.0 cm) anemones collected for surface-area measurements were similar (P > 0.05, Table 2). Although a positive trend of more tentacles with increasing basal disc diameter was found, no significant regressions of these two variables were obtained. Sebens (1981a) has shown that tentacle number increases over the lower range o f body mass in this species. Tentacle crown, total tentacle and total prey- capture surface-areas were significantly larger in L anemones of any basal disc diameter (Table 2, Figs. 2 and 3). No significant differences between H and L anemones were found in comparisons o f the other surface-area regressions, and these data have been pooled.

Tentacle surface-area can be predicted from basal disc diameter using the equations of this study (Table 2) or the

equations of Sebens (1981a) which relate ash-free dry weight (AFDW) to basal disc diameter, and tentacle surface-area to AFDW. For an anemone of 3.0 cm basal disc diameter, predicted tentacle surface-area using Se- bens' equations (47.2 cm 2) is similar to values obtained using the present equations for H (45.3cm 2) and L (51.7cm 2) anemones (assuming mass fraction o f a s h = 0.10). However, the regressions of reduced weight vs basal disc diameter and dry weight vs reduced weight were different for H and L anemones (Fig. 4). High-intertidal anemones generally had a smaller dry mass than L anemones of any disc diameter (Fig. 5). Hence, a plot of total prey-capture surface-area vs anemone dry weight (Fig. 6) shows that high- and low-intertidal anemones had similar surface-areas relative to mass (intercepts of regressions of square root of prey-capture surface-area vs log dry weight are equivalent, P=0.358) , despite the significant differences relative to basal disc diameter.

Dry body weight and total prey-capture surface-area per gram dry weight were computed for H and L anemones of 1.7 cm basal disc diameter (Table 1), to emphasize the different body weights and similarity in surface-area index relative to the difference in weight of prey. Dif- ferences in surface area consequently contributed little to observed differences in coelenteron contents.

304

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k- z 3O i,i k-

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H i g h I n t e r t i d a l �9

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T e n t a c l e S . A , = 5 . 3 2 D 2-16

R 2= 0 . 8 2

N = 2 0

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1.O

W. E. Zamer: Physiological energetics ofAnthopleura elegantissima. I.

L / o

�9

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T e n t a c l e S.A.= 4 . 4 5 D 2"10

R 2 = 0 .73

N - - 2 4

I I ! I

1.4 1.8 2 .2 2.6

B A S A L DISC D I A M E T E R ( c m )

I I

3.0 3.4

Fig. 2. Anthot)leura elegantissima. Total tentacle surface-area (S.A.) vs basal disc diameter in high(H)- and low(L)-intertidal anemones. Lines fitted using predicted points from the power curve equations. See Table 2 for results ofcovariance analysis

Absorption efficiencies

High-intertidal anemones had a significantly greater gravimetric absorption efficiency than did low-intertidal ones (Table 3). Both acclimation regime and original tidal position significantly affected absorption efficiency in the Orono cross-acclimatization experiment. High-intertidal anemones had greater efficiencies regardless of ration size (P=0.019), but increasing ration led to lower efficiencies for both H and L anemones, as shown in the comparison of I and S treatments (P < 0.0001). This comparison does not eliminate the possibility that aerial exposure per se could have altered the efficiencies. Transfer of subtidally acclimated anemones to intertidal conditions resulted in a sharp drop in absorption efficiency for both H and L anemones on the first day of transfer because of an inability to retain food in their coelenterons upon acute

emersion (Fig. 7). However, by the end of five days these anemones had the same absorption efficiencies as controls, indicating that aerial exposure probably does not affect absorption efficiency on a long-term (> 5 d) basis. Thus, differences in rations, not physical conditions, led to the absorption efficiency differences in the Orono experiment. At 1% ration, both H and L anemones increased absorption efficiency further (85.5 and 81.9%, respectively) and H anemones still absorbed more (P = 0.037).

Ash content of adult Artemia sp. (0.046 of dry weight; Table 4) was similar to the value of 0.043 reported by Coles (1969). Using the standard conversion of 4.186J ca1-1, weight-specific energy content predicted by the CHN stoichiometric concept (26.930kJg -1) becomes 6.433 kcal g-i, which is higher than 5.834 and 5.854 kcal g-~ reported by Coles (1969) and Paffenh/3fer (1968), respectively, for Artemia sp. nauplii.

Table3. Anthopleura elegantissima. Absorption efficiencies for Orono and Bodega Harbor experiments. Gravimetric efficiencies are grand means ( f ) of daily efficiencies over 15 d (Orono) and 10 d (Bodega Harbor) for the number of experimental individuals (N). L1 and L2 are lower and upper 95% confidence limits. P values are from two-way (Orono) and one-way (Bodega Harbor) ANOVA. Carbon, nitrogen, organic and energetic efficiencies have been computed from Eq. (1) and the per- tinent mean values from ashing and CHN analysis (Tables 5 and 6)

Experimental Ration treatment (% body wt)

Absorption efficiencies (%)

F L1 L2 N

Gravimetric Organic C N Energetic

Orono

HI 4.0 81.0 HS 5.6 63.5 LI 4.0 76.1 LS 5.6 58.0 Tidal height P = 0.019 Acclimation P = 0.0001 Interaction P = 0.9939

Bodega H 1 L 1

78.9 83.4 15 84.7 85.9 88 .0 85.6 56.9 70.4 12 72.8 73.7 80.0 72.6 70.8 81.7 9 79.7 80.4 84 .4 79.8 53.6 62.5 l0 66.4 67.9 75 .2 67.1

85.5 81.9 P = 0.037

80

82.8 88.1 6 92.5 94.8 94.2 95.5 79.3 84.6 6 90.0 91.8 91.4 92.1

70

10

6O oq

E

,,, 50 r,,..

LI.I (J

4 0

O3

W e r

3o

>-

W a: 20 e~

g"

Low I n te r t i da l O

High In te r t i da l �9

PCSA =8,74 D 1"74 L

R2=O.79

N=19 �9

�9 i

.,i, Q

1.0

~ '0 �9


I i r i i B i |

1.4 1 .8 2 .2 2 . 6

O O

PCSA= 5.87 D 1"93

R2=O.78

N = 2 2

I l l l l

3 .0 3 .4

BASAL DISC DIAMETER ('cm)

Fig. 3. Anthopleura elegantissima. Total prey-capture surface-area (PCSA) vs basal disc diameter in high- and low-intertidal anemones. Lines as in Fig. 2. See Table 2 for results of covariance analysis

Results o f ashing and CHN analysis (Tables 4, 5 and 6) were used to calculate total organic, carbon, nitrogen and energetic absorption efficiencies. Removal of carbon and nitrogen from the ration was more efficient in H anemones compared to L anemones (Table 3). This result is not due simply to greater gravimetric absorption efficiencies in H anemones, which are incorporated in the calculations for carbon and nitrogen absorption, but to greater weight- specific removal of carbon and nitrogen as well (Table 6). Therefore, energy content of egesta from H anemones was comparatively low, which resulted in higher energetic absorption efficiencies. The patterns o f differences among the treatments in energetic, carbon, nitrogen and organic absorption efficiencies are similar to that of the gravimetric efficiencies.

Digestion rates

First appearance of egesta occurred as early as 3.5 h following ingestion in 4 o f 12 H anemones and 3 o f 10 L anemones. By 4.5 h following feeding, 11 of 12 H anemones and 6 of 10 L anemones had produced egesta. All anemones had produced egesta by 5 h. At 7 h all H anemones had stopped egestion; L anemones continued egestion for approximately another hour.

Net growth efficiencies

The average ratios of reduced weight in seawater to reduced weight in distilled water were 0.490-t-0.103 (SD)


E

l-

W

Q L~

Q L~J e~

1 0 0 0

500

100

50

| I I I I 101 2 3 4 S 6

BASAL DISC DIAMETER(cm)

A

L: log(Reduced Wt)= Low Intert idal o 2 .003.1og(BasalDisc Diameter) High Intert idal �9 +1.353

o o

1100 L: Iog(DryWt )=1 .017 - / lOOO log(ee~ueed wt 1 / /

/ ~ / ~ 800

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~ i ~" / �9 Iog!DryWt)= ~r s o o >" ~ �9 1.017"log{Reduced Wt ) ee

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II �9 / ~ log(Reduced W t ) = 0 90 100 150 200

/ �9 2,003"log(Basal Disc Diameter) REDUCED WEIGHT (rng)

+1 ,239 Fig. 4. Anthopleura elegantissima. (A) Reduced weight (weight in sea water) vs basal disc di-

e ameter; lines fitted using predicted points from the linear regressions; both regressions are significant (P < 0.0001); H: R z = 0.660, N = 25; L: R 2 = 0.699; N = 22; analysis of covariance indicates that although intercepts are not significantly different, probability level (P < 0.0508) is near the critical level (0.05); pooled slopes are shown. (B) Whole-anemone dry weight vs reduced weight in high- and low-intertidal anemones; lines as in (A); both regressions are significant (P<0.0001); H: R2=0.914; N = 18; L: R2 =0.967; N= 18; analysis of covariance indicates that intercepts are significantly different (P < 0.0003)

2000

1500

E

1000

w z o

w z

500

Low Intertidal 0 /

High Intertidal �9 / /

o o

L 0

W= 133.51 D 1.91 R2= 0.80 / 0 N =20 0

O O O /

O / � 9 1 4 9 O O O

�9 / i i o

0 Y �9 W= 65.29 D 2.24 �9 R2=0.66

. .=24

1'.2 ' 116 ' 210 ' 2:4 ' 2:8 ' 312 ' 3;6 ' 4'.0 ' BASAL DISC DIAMETER (cm)

414

Fig. 5. Anthopleura elegantissima. Whole-anemone dry weight vs basal disc diameter in high- and low-intertidal anemones. Dry weight was calculated from basal disc diameters using equations in Fig. 4. Lines as in Fig. 2


80

f-%

60

< W m 511

~9

W

[ 3o <

>. W ~ 2c

High I n t e r t i d a l � 9

Low Inter t ida l o P C S A = 0 . 2 1 W O'82

R2=O,78

N = 2 2

�9 0

0

16o

Z O 0 ~

0

O O

/ / / / L

PCSA = 0.14 W 0"87

R2=0.79

N = 1 9

560 ' 960 ' 13'00 A N E M O N E DRY WT ( m g )

Fig. 6. Anthopleura elegantissima. Prey-capture surface-area (PCSA) vs dry weight in high- and low-intertidal anemones. Dry weight was calculated from basal disc diameters shown in Fig. 3 using equations in Fig. 4. Covariance analysis of the square root of PCSA vs log10 dry wt indicates no difference between intercepts (P<0.358); H-intercept: 2.716; L-intercept: 2.508; pooled slope = 0.0068. Regression of the pooled data of both groups is significant (P< 0.0001); R 2 =0.813

and 0.490_ 0.079 for pre- and post-experimental H anemones, respectively (N=7). Corresponding values for L anemones were 0.413 • 0.100 (SD) and 0.420 +_ 0.106 (N= 8). In neither case was the difference between the pre- and post-experimental ratio significantly different from zero (Student's t-test; P=0.235, P=0.844, respectively). Thus, major density changes did not occur, and the same equation can validly be used to predict dry weights from reduced weights at tlie beginning and end of the experiment.

Gravimetric net-growth efficiencies (/<2) were greater for high-intertidal anemones than for low-intertidal anemones (Table 7) regardless of experimental treatment, as seen in the Orono results (P = 0.028). However, the effects of ration size were more complicated: ration was positively correlated with /<2 for H anemones and negatively correlated for L anemones. Thus, the effect of ration size on gravimetric /(2 appears to depend on original tidal position (interaction P<0.036). Conversely, energetic net- growth efficiencies are similar for the four treatments in

Table 4. Artemia sp. Results ofashing and CHN analysis of ration. Ashr, Mean_+SD (N), is ash fraction based on two replicates, one each of oven-dried (60 ~ and freeze-dried samples, fCr and fNr are fractions of total carbon and nitrogen, respectively; wc and wn are organic mass fractions of carbon and nitrogen, respectively, derived from three replicate determinations on freeze-dried samples. Energy content of organic fraction of food, Er, is in units of kJ (g organic wt) -1

Ashr fCr fNr Wc wn Er

0.046_+0.004 0.550_+0.002 0.095_+0.000 0.570 0.100 26.930 (2) (3) (3)

100

90

80 >- 0 Z

70 0 U. U. LU 60

Z o F- so EL n- O Or) 40 O0 <

3O

I_

. . . . Contro ls �9

- - Acu te Transfer o

LI " x \

HS , - - - - - - - ' ~ -'-~7%///~ . / " \ . ~ - . / / / - ~ _ . , .

HS

LS

I ! ! i i 1 2 3 4 5

D A Y S A F T E R T R A N S F E R

Fig. 7. Anthopleura elegantissima. Time course of changes in gravimetric absorption efficiency following acute transfer of experimental specimens to alternate tidal regime without changing ration. I: intertidal acclimation; S: subtidal acclimation (original conditions). Each point represents mean daily efficiency for not less than five anemones, except LI controls (N= 4). Error bars have been omitted for clarity; standard deviations ranged from 20 to 24% of control means, and from 12 to 33% of acute means over 5d

Tab

le 5

. An

thop

leur

a el

egan

tissim

a. R

esul

ts o

f as

hing

and

CH

N a

naly

sis

of b

ody

tiss

ues

and

eges

ta f

rom

Oro

no e

xper

imen

t.

Mea

ns -

+ S

D (

N =

num

ber

of a

nem

ones

). P

val

ues

are

from

tw

o-w

ay A

NO

VA

s. S

ingl

e su

bscr

ipt,

e,

deno

tes

eges

ta;

dual

sub

scri

pts,

te

and

tb,

den

ote

tiss

ues

of w

hole

ane

mon

es a

t th

e en

d an

d be

ginn

ing

of t

he e

xper

imen

t; W

c an

d W

n ar

e or

gani

c m

ass

frac

tion

s of

car

bon

and

nitr

ogen

for

ege

sta.

Oth

er s

ymbo

ls a

nd u

nits

as

in T

able

4

Exp

erim

enta

l A

she

Ash

te

Ash

tb

fCe

fNe

trea

tmen

t W

c W

n E

e E

tb

Ete

HI

0.23

1_+0

.037

0.

074-

-+0.

007

0.08

9-+0

.001

0.

409+

0.01

5 0.

060-

+0.

007

0.53

1-+

0.01

9 0.

077-

+0.

009

24.5

41-+

1.26

8 20

.830

--+

0.07

823.

241-

+0.

665

(6)

(8)

(4)

(4)

(4)

(4)

(4)

(4)

(3)

(3)

HS

0.

289-

+0.0

24

0.08

4-+

0.00

4 0.

094-

+0.

007

0.39

7-+0

.011

0.

052_

+0.0

02

0.55

8-+0

.015

0,

073-

+0.

003

26.2

05-+

1.00

1 20

.726

-+0.

277

23.4

06-+

0.83

9 (6

) (6

) (4

) (6

) (6

) (6

) (6

) (6

) (3

) (4

)

LI

0.19

0-+0

.028

0.

074_

+0.0

01

0.08

5-+

0.00

9 0.

451_

+0.0

32

0.06

2_.+

0.00

6 0.

557-

+0.

039

0.07

6-+

0.00

7 25

.901

-+2.

581

20.1

52-+

0.13

8 22

.842

-+0.

369

(4)

(3)

(3)

(4)

(4)

(4)

(4)

(4)

(2)

(4)

LS

0,23

8-+0

.016

0.

075-

+0.

009

0.09

5-+

0.00

4 0.

421-

+0.

013

0.05

6+_0

.005

0.

552-

+0.

017

0.07

4+_0

.007

25

.574

-+1.

091

21.1

15-+

0.08

5 24

.672

-+0.

854

(3)

(6)

(3)

(4)

(4)

(4)

(4)

(4)

(3)

(2)

Tid

al h

eigh

t P

= 0.

1171

P

= 0.

0020

P

= 0.

1868

P

= 0.

3857

P

= 0.

9504

P

= 0.

6293

P

= 0.

2059

P

= 0.

2965

A

ccli

mat

ion

P =

0.08

95

P =

0.03

24

P =

0.01

50

P =

0.33

82

P =

0.28

76

P =

0.38

11

P =

0.00

43

P =

0.03

12

Inte

ract

ion

P =

0.17

95

P =

0.31

07

P =

0.67

72

P =

0.17

50

P =

0.79

48

P =

0.19

94

P =

0.00

13

P =

0.06

22

Tab

le 6

. An

thop

leur

a el

egan

tissim

a. R

esul

ts o

f as

hing

and

CH

N a

naly

sis

of b

ody

tiss

ues

and

eges

ta f

rom

Bod

ega

Har

bor

expe

rim

ent.

Mea

ns_

SD

(N

= n

umbe

r of

ane

mon

es).

P

valu

es

are

from

one

-way

AN

OV

As.

Ash

e va

lues

are

mea

ns o

f tw

o re

plic

ates

ofe

gest

a co

mbi

ned

from

six

indi

vidu

als

in e

ach

trea

tmen

t. A

ll o

ther

sym

bols

and

uni

ts a

s in

Tab

les

4 an

d 5

N

~z

Exp

erim

enta

l A

she

Ash

te

Ash

tb

fC e

fN

e W

c W

n E

e E

tb

Ete

tr

eatm

ent

H

0.50

4+0.

012

0.10

0+0.

004

0.08

7___

0.00

9 0.

198+

0.01

3 0.

038+

0.00

2 0.

397+

0.02

6 0.

076+

0.00

3 15

.552

+1.

762

21.1

45__

+0.7

99

(2)

(6)

(8)

(6)

(6)

(6)

(6)

(6)

(8)

L

0.47

2•

0.08

4+0.

002

0.08

7+0.

007

0.24

8•

0.04

5•

0.46

8+0.

037

0.08

5+0.

007

20.4

29__

+2.

474

21.1

24-+

0.93

7 (2

) (6

) (8

) (6

) (6

) (6

) (6

) (6

) (8

)

P=

0.

1578

0.

0001

0.

9637

0.

0003

0.

0015

0.

0029

0,

0194

0.

0028

0.

9620

22.0

50_+

0.10

8 (6

) 21

.965

_+ 1

.143

(6

) 0.85

99

o �9

W. E. Zamer: Physiological energetics ofAnthopleura elegantissima. I. 309

Table 7. Anthopleura elegantissima. Gravimetric and energetic net growth efficiencies (/(2) and average daily growth in anemones from Orono and Bodega Harbor experiments. Daily growth is expressed as percent change in dry weight relative to initial dry weight per day; Orono experiment ran for 14 d; Bodega experiment ran for 6 d. Values are means,+ SD; (N)= number of anemones. L1 and L2 are lower and upper 95% confidence fimits, respectively. P values are from a two-way ANOVA. Energetic/(2 was calculated from mean values in Tables 4, 5 and 6. -: no data

Experimental Initial Daily K2 (%) treatment body wt growth

(g) (%) Gravimetrie Energetic

2 L1 L2 2 LI L2

Orono HI 0.449,+0.124 1.48_+0.34 45.1 38.8 50.9 57.6

(15) (15) (15) (14)

HS 0.493,+0.166 1.82,+0.56 52.6 46.1 59.0 58.4 (12) (12) (12) (II)

LI 0.351_+0.105 1.37,+0.49 44.6 33.7 55.3 58.2 (9) (9) (9) (9)

LS 0.338_+0.143 1.16_+0.40 37.2 27.8 46.1 61.1 (10) (10) (10) (8)

Tidal height P = 0.0104 0.0285 0.4567 Acclimation P = 0.7835 0.9917 0.4080 Interaction P = 0.0637 0.0363 0.6338

Bodega H 0.987+0.238 0.63-+0.52 28.0 6.58 51.8 35.2

(6) (6) (6) (6)

L 1.549 + 0.526 - 1.17,+ 0.26 - growth - - - growth (6) (6) (6) (6)

53.9 61.3

54.2 62.6

53.5 62.8

56.2 65.9

18.6 52.4

the Orono experiment, indicating no correlation between ration and /s Thus, LS anemones were as efficient as individuals from the other treatments at storing energy in their body tissues, despite being the least efficient at adding body mass. The effects o f aerial exposure on K2 have not been described in this species. Anemones fed 1% rations had lower growth efficiencies (Table 7) than those fed 4.0 or 5.6% rations. In fact, L anemones fed 1% rations lost an average of 1.2% dry body weight each day despite a slight increase in weight-specific energy content of body tissues (Table 6). Tissue energy-content o f H anemones also increased during the experiment. Energetic K2 is consistently higher than gravimetric values in both experiments.

Average daily growth was significantly dependent on original shore position (Table 7), H anemones adding 1.5 to 1.8% and L anemones adding 1.2 to 1.4% dry body weight per day under large ration conditions. High- intertidal anemones added 0.6% to their mass each day when fed 1% rations.

Discussion

Prey capture

High-intertidal individuals o f Anthopleura elegantissima partially compensate for the habi tat- imposed reduction in feeding time by small but significant increases in food-

absorption efficiency and much larger increases in prey capture and ingestion rates compared to low-shore anemones. Nevertheless, L anemones capture more prey daily than do H anemones because of more time available for feeding (Zamer, in preparation).

The threefold greater weight o f prey in coelenterons of H anemones could have arisen from greater prey availability in the upper intertidal zone, slower digestion rates (longer throughput times) in high-shore anemones, a short immersion (feeding) period relative to coelenteron residence time in H anemones, or higher prey capture rates in H anemones.

Anemones used in coelenteron-content measurements were collected during ebbing tides on two days. The same pattern of results was seen the previous year in a prelimi- nary experiment in which anemones of similar size were collected but basal disc diameters were not measured [mean prey weight_+ SD (N); H: 2.1 _+ 1.2 mg (3); L: 1.2 mg (2)]. Time available for feeding is predictable for an intertidal invertebrate, but food availability may be un- predictable because of patchy distributions of food. The quantity of prey in coelenterons of individuals of Antho- pleura elegantissima is extremely variable, as is that of Metridium senile (Sebens and Koehl, 1984). These data reflect the stochastic and opportunistic nature of feeding in passive suspension feeders. The present collection site was at the mouth of Bodega Harbor, where substantial water mixing occurs because of boat movements as well as tidal flow. Although a difference in prey availability cannot be


eliminated as a cause of the coelenteron-content differences, higher prey-capture rates by high-shore anemones appears to be more likely given such water mixing and observations of receptivity to prey (see below).

Nor is the large difference in coelenteron content likely to be due to either slower digestion rates or short feeding periods relative to residence-time of prey in the coelenteron of H anemones, both of which could lead to increased prey weights. Throughput times (Sibly, 1981) are the same (approximately 4 h) in H and L Anthopleura elegantissima, despite somewhat higher air temperatures (13 ~ to 19~ to water temperatures (11 ~ to 13~ Increased temperature decreases throughput time in colonial hydroids, for example (Kinne and Paffenh6fer, 1965). Four hours is similar to times reported for another sea anemone, Metridium senile (2 to 4 h; Sebens and Koehl, 1984) and siphonophores (2 to 3 h; Biggs, 1976; 1.6 to 9.6h; Purcell, 1983). High-intertidal anemones were collected for these measurements following a shorter immersion period than that experienced by L anemones. However, this does not mean that prey residence time was shorter in H anemones compared to L anemones. In- dividuals from both shore positions were immersed for more than 6 h, longer than throughput time and nearly as long as extreme residence time of prey in the coelenterons (7 to 8 h). Thus, even if initial prey-capture rates were high and declined with time, most prey captured by H anemones immediately after immersion would not be likely to be present in coelenterons at emersion. Partially digested prey, captured soon after immersion and remaining in H anemones, probably accounts for little of the large difference in prey weight.

The possibility remains, however, that L anemones had higher initial rates of prey capture than those inferred from prey weights at the end of immersion. Using the static quantity of weight of prey, and the throughput time may underestimate prey capture and ingestion rates. This subject has ben reviewed briefly by Calow (1977 a). Mur- taugh (1984) has shown that throughput times are inversely related to ingestion rates in the mysid Neomysis mercedis. Likewise, ingestion rates are higher and throughput times concomitantly shorter in three species of deposit-feeding polychaetes when the worms are offered food richer in protein than that offered to control individuals (Taghon and Jumars, 1984). Continuous feeding in L anemones under natural conditions could lead to throughput times shorter than the 4 h measured using a periodic feeding regime. Therefore, feeding and ingestion rates may he underestimated. High-intertidal anemones on the other hand are restricted to a moreper iodic feeding regime, so that throughput times measured under experimental conditions may accurately reflect naturally oc- curring values. This particular point cannot be resolved until methods are developed which allow direct measurement of prey capture rates under conditions approximating natural ones.

Although the data are not convincing, the simplest explanation for differences in coelenteron content is higher

prey-capture rates in high-shore anemones. Since Sebens (1981a) has shown that prey capture is directly related to feeding (tentacle crown)-surface area in this species, increased rates of prey capture in H anemones might arise from larger feeding surfaces compared to L anemones. However, total prey-capture surface-area is the same in H and L anemones of similar mass (Fig. 6). From observations made soon after collection, high-intertidal anemones exhibit greater tentacle movement and consistently ingest presented prey more quickly than L anemones (own unpublished observations and J. M. Shick, personal communication), supporting the interpretation of higher ingestion rates in H anemones. Similar observations were made by Sandberg et al. (1971) and Mariscal (1973), who showed that sensitivities of nematocyst discharge are reduced after feeding in the anemones Calliactis tricolor and Epiactisprolifera. Ingestion of food totalling only 3 to 6% of body weight resulted in noticeable decreases in the sensitivity of discharge in the former species. These authors also noted stretching of tentacles and increased tentacle waving in starved anemones, which may indicate generally greater receptivity to prey. Nematocyst discharge in Hydra spp. may be mediated by enzymes involved in energy metabolism (Lentz and Barrnett, 1962), perhaps implying a physiological link between nutritional status and prey-capture capability for cnidarians in general.

Longer feeding time in low-intertidal individuals of Anthopleura elegantissima probably leads to a nutritional state closer to satiation and a concomitant reduction in sensitivity of nematocyst discharge. High-intertidal individuals will probably be further from satiation upon reimmersion because of continued digestion and depletion of previously captured prey during aerial exposure, and because they capture less prey daily than do L anemones. Thus, although greater weights of prey in coelenterons of H anemones reflect greater ingestion rates, they do not reflect overall nutritional status: H anemones are under- nourished compared to L anemones because of shorter feeding time.

Few intertidal invertebrates are known to increase rates of energy acquisition following emersion, and all of the known examples are active feeders. Upon immersion, high-intertidal individuals of Littorina littorea increase grazing rates (Newell et al., 1971), and the bivalve Lasaea rubra increases initial filtration rate relative to low-intertidal individuals (Morton et al., 1957). Gillmor (1982) has predicted that high-intertidal individuals of the mussel Geukensia demissa acclimate rate functions (perhaps filtration rate), thereby maintaining higher growth rates than low-intertidal individuals. Although intertidally acclimatized individuals of the bivalve Cardium edule exhibit higher initial rates of filtration than subtidally acclimatized ones, similar treatment of Mytilus edulis elicits no such response (Widdows and Shick, 1985). Finally, individuals of the bivalve Choromytilus meridionalis do not increase filtration rate after aerial exposure (although an abnormally long exposure period does result in increased filtration rate) (Gfiffiths and Buffenstein, 1981).


Passive suspension-feeders such as A nthopleura elegantissima cannot change filtration rate by changing ciliary activity. Instead, these anemones must rely on other behavioral (tentacle waving) or cellular (nematocyst discharge) adaptations to increase prey-capture rate, barring changes in surface area. But the condition required to elicit increased receptivity to prey appears to be a decrease in total daily ration, so that only H anemones respond via increases in tentacle waving and, perhaps, sensitivity of nematocyst discharge. Given this mechanism, one also might expect differences in ingestion rate on the basis of values for the contribution of zooxanthellae to animal respiratory requirements (CZAR; Muscatine et al., 1981). CZAR was estimated to be 18% in H anemones and 34% in L anemones (Shick and Dykens, 1984).

Absorption efficiency

Absolute values for absorption efficiency in Anthopleura elegantissima are within the range of Previously reported values for Actinia equina (Ivleva, 1964) and other aquatic carnivores (Welch, 1968), but are substantially higher than those reported by Hunter (1984) for individuals of the anemone Aiptasia pulchella, which were fed much larger rations than those used in the present experiments.

Increases in energy acquisition may be accomplished by adjustments in absorption efficiency also. However, absorption efficiency is inversely related to ingested ration in H and L individuals of Anthopleura elegantissima. This inverse relationship has been demonstrated in other marine invertebrates such as the bivalve Aulaeomya ater (Griffiths and King, 1979), the ctenophores Pleurobrachia baehei and Mnemiopsis mceradyi (Reeve et aL, 1978) and the hydroid Clara muItieornis (Paffenh6fer, 1968).

Lower ingestion rates in continuously fed L anemones on the shore are perhaps matched with maximum absorption efficiencies. Alternatively, the larger daily ration in L anemones might lead to a lower efficiency. Neverthe- less, absorption efficiency is slightly but consistently higher in H anemones regardless of ration level. Aerial exposure per se does not affect absorption efficiency in these anemones, and all experimental individuals were fed once each day so that continuous feeding in L vs intermittent feeding in H anemones could not have led to these differences. Regardless of the explanation (see below), increased absorption efficiency increases energy acquisition in H anemones and therefore represents an adaptive response.

Growth

The generally higher growth rates and net growth efficiencies (K2) in H anemones fed rations approximating natural ones may be due to a reduction in metabolic costs when H anemones are exposed to air compared to L anemones of similar size (Shick and Dykens, 1984). Dur- ing aerial exposure, intertidally acclimatized individuals of

Anthopleura elegantissima remain fully aerobic (Shick and Dykens, 1984), and therefore the decrease in rate of oxygen uptake in A. elegantissima reflects a decline in total metabolic demand. A reduction in metabolic costs during aerial exposure is a common response of intertidal invertebrates and is part of a conservationist "strategy" outlined by Branch and Newell (1978). A consequence of this strategy is increased energy available for growth and reproduction (compared to energy that would be available without such a metabolic reduction) despite reduced feeding time (Widdows and Shick, 1985; Zamer, in preparation).

Higher energetic K2 values vs gravimetric ones imply preferential incorporation of energy-rich, less dense lipids into new tissues compared to carbohydrates and proteins. Additionally, the energetic efficiency appears to be maxi- mized at approximately 60% when food availability is high (Table 7). This average value is very high compared to those of other aquatic carnivores (Welch, 1968), and this result appears related to the fact that anemones are sit- and-wait predators having virtually no locomotory costs involved in prey capture. However, the 35.2% efficiency exhibited by H anemones fed more realistic amounts of food is not unusual compared to other animals (Conover, 1978), hence it is surprisingly low for the same reason. The value would be even lower if energy from the algal symbionts were included in the calculation. The growth efficiency data imply, therefore, that a substantial proportion of the absorbed ration is being utilized to support costs or production not directly measured in this study. Mucus production is probably an important component of the energy budget of these anemones (Zamer, in preparation). Mucus may account for 20% (freshwater gastropods) to 70% (flatworms) of ingested ration (Calow, 1977 a).

Growth rates and growth efficiencies are generally inversely related to body size (reviewed by Calow, 1977 b), but gravimetric and energetic/s do not vary consistently with body size in Anthopleura elegantissima (Table 7). L anemones were larger than H anemones in the Bodega Harbor experiment, but the opposite is true of the Orono experiment (although the range is small). Larger anemones have greater daily metabolic costs than smaller ones. Thus, the difference in growth between H and L anemones used at Bodega Harbor may be explained in part by the difference in mean weights. However, if size alone determined differences in growth rates and efficiencies, L anemones used in the Orono experiments should have grown faster than H anemones. They did not, evincing the effect of original shore position (P--0.0104; Table7). Increased temperature may result in higher growth rates (e.g. Paffenh6fer, 1968), but air and seawater temperatures at Bodega Harbor are similar throughout most of the year (Sutherland, 1970; Barbour etal., 1973), and both were held at 15 ~ in the Orono experiment.

Finally, higher absorption and net growth efficiencies in high- vs low-intertidal specimens of Anthopleura elegantissima which cannot be erased by acclimation to common conditions may be due either to genetic or to


irreversible nongenetic differences. Correlations among genotype frequency, individual body size and current regime have been demonstrated in Metridium senile (Shick et al., 1979 b), and genetic differences have been correlated with differences in frequency distributions relative to intertidal height in two color morphs of the anemone Actinia equina (Quicke etal., 1983). Irreversible nongenetic physiological changes can be experimentally in- duced in sea anemones (Zamer and Mangum, 1979) and have been proposed as an explanation for morphological differences among clonemates ofAnthopleura elegantissima (Francis, I976). Causes for the differences in efficiencies await further study.

Effects of exposure to air on allometric relationships

Larger body size is directly related to fitness in an animal such as Anthopleura elegantissima in which volume of. gametes produced is directly related to body size (Sebens, 1979, 1981b, 1983). Yet increases in body size are restricted as time available for feeding decreases in the upper intertidal zone. Adaptations which result in more energy available for growth and reproduction, mitigating the effects of reduced feeding time, will be selectively favored. The capacity of H anemones to grow when food availability is low represents improved fitness of these specimens compared to that of L anemones maintained under similar conditions. Higher growth rates in H anemones will lead to attainment of the minimum body sizes necessary for both asexual and sexual reproduction (Se- bens, 1980; 1981a, b; 1982b) in a shorter period of time and despite assimilating less energy each day than L specimens (Zamer, in preparation). The higher growth rates are supported by higher rates of prey capture and reduced metabolic rates.

A full appreciation of differences in prey capture in high- and low-intertidal individuals of Anthopleura elegantissima cannot be realized in an energetic context without noting that basal disc diameter is a better pre- dictor of mass if intertidal position is considered. Low- intertidal anemones consistently have a larger body mass compared to high-intertidal anemones of any basal disc diameter. Yet prey-capture surface-areas per gram body mass are the same in individuals from these two groups. The greater relative mass of L anemones appears to be related to longer feeding time, since the differences in the relationships of reduced weight to dry weight can be erased and even reversed with acclimation to common laboratory conditions (Zamer, unpublished data).

High- and low-intertidal individuals of Anthopleura elegantissima exhibit higher routine metabolic rates when fed ad libitum in the laboratory compared to freshly collected individuals, and metabolic rates in freshly collected H anemones are lower than in L anemones (Shick, 1981). However, cross-acclimatization of H anemones to subtidal conditions and L anemones to intertidal conditions reverses the pattern of aerobic metabolic rates (Shick,

1981). Additionally, tissue energy-content rises under laboratory conditions compared to values in specimens freshly collected from both shore positions. Thus, the larger daily ration of L anemones appears to be correlated with larger relative mass and higher rates of standard metabolism. A similar situation exists in some marine fishes. Compared to species in shallower water, bathypelagic fishes have less organic mass and lower standard rates of metabolism, two characteristics which have been correlated with their energy-poor environment (Childress and Somero, 1979).

PreY-capture surface-area increases with body size (weight exponent, b = 0.54), but respiratory losses increase with a greater power of body mass (b=0.77) in continuously immersed anemones (Sebens, 1981 a). The difference in exponents leads to the prediction of a maximum body size for Anthopleura eIegantissima beyond which respiratory costs outstrip prey-capture capabilities (Sebens, 1980, 1981a, 1982a, 1983). In this context, high-intertidal anemones may attain a distinct energetic advantage upon reaching a larger size compared to low-intertidal individuals. Although H and L anemones were not exam- ined separately in their study, Shick etal. (1979a) have demonstrated that weight-specific rates of oxygen uptake in aerially exposed A. elegantissima are much more weight-dependent (weight-specific slope, b-1=-0.623) than aquatic rates (b-I =-0.166). Thus, a relatively large H anemone that is aerially exposed for 14 h each day will have an absolute daily respiratory cost which is somewhat higher than that of a smaller H anemone under the same exposure conditions, and which is much lower than that for an L anemone of similar size experiencing much shorter emersion periods. Therefore, unlike L anemones, the prey-capture surface-area of aerially exposed anemones may increase as a greater power of body weight (b=0.54 to 0.85, Sebens, 1981a and present Fig. 6, respectively) than respiratory costs (b=0.38 in air; Shick etal., 1979a). The different weight exponents of prey- capture surface-area may be due to postural differences between anemones photographed in still water (present study) compared to flowing water (Sebens, 1981a). Ad- ditionally, the different exponents may reflect morphometric differences between anemones collected from a protected site (Bodega Harbor) compared to an exposed, outer coast site (Tatoosh Island, Washington; K. P. Sebens, personal communication). Nevertheless, both exponents are substantially larger than the weight exponent for aerial respiration.

High-intertidal anemones may approach sizes com- parable to those of low-intertidal anemones because of these allometric relationships, and despite shorter feeding time and decreased CZAR (Shick and Dykens, 1984). Sebens' (1983) data show that size distributions of H anemones overlap those of L anemones at a number of sites on the Washington coast, and that rates of increase in clonal biomass are not strongly dependent on intertidal position. Additionally, size of H anemones at a single tidal height (same feeding time) is inversely related to the maximum temperatures reached in tide pools during low


tide (Sebens, 1980). Higher temperatures lead to higher metabolic rates. At Bodega Harbor, where most of the anemones are on open rock faces and air and seawater temperatures are similar, daily metabolic costs of H anemones are smaller than those of L anemones. Thus, partial compensation for the effects of reduced time available for feeding appears to occur in a number of populations o f this species. However, weight loss will result if increases in exposure time and/or decreases in zooplankton concentration are greater in magnitude than the compensatory capacity of the organism to increase prey- capture rate or reduce metabolic costs. This is clearly the case for anemones at the upper distributional limit, where Anthopleura elegantissima are significantly smaller than low-shore individuals (Sebens, 1981b, 1983). Yet, somewhat lower in the upper intertidal zone anemones do attain sizes approaching those o f individuals lower in the intertidal, in part because of adaptations demonstrated in this study.

Acknowledgements. I am grateful to Dr. J. M. Shick, for his encouragement, guidance and enthusiasm for the research presented here, and for critically reading the manuscript. I also thank Drs. J. Dearborn, B. Sidell, J. Ringo, R. Vadas and H. Dowse for technical assistance.. All of these individuals and Drs. R. J. Hoffmann, J. M. Lawrence, K. P. Sebens and an anonymous reviewer made useful com- ments on various stages o f the manuscript. I thank Drs. W. Haltemann for advice on the use of the Statistical Analysis System: E. Gnaiger for advice on CHN analysis and use of the stoichiometric equations; and L. Bookbinder for assistance. Useful discussions were had with all o f the above individuals and Dr. J. Dykens. Thanks to E. Meisner, M. Nims and F. Wing for typing, T. Veilleux for excellent technical support and S. Watkins for Fig. 1 drawings. Additionally I thank the staff of the Bodega Marine Laboratory, University o f California particularly N. Stim- son, P. Sirri and Dr. C. Hand; the staff of the Institute for Marine Environmental Research in Plymouth, England, particularly Drs. P. Watkins, A. J. S. Hawkins, and B. L. Bayne; and L. Schick of the Ira C. Darling Center of the University of Maine, all of whom provided help and hospitality during my stays at their institutions. This research was supported by a National Science Foundation Grant to J. M. Shick (PCM79-11027; Regulatory Biology), and by grants from the Graduate Student Board, the Migratory Fish Research Institute, the Center for Marine Studies and Zoology Department, all of the University of Maine at Orono; and by the Department of Biology, Bowdoin College.

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Date of final manuscript acceptance: April 25, 1986. Communicated by J. M. Lawrence, Tampa

physiological energetics of the intertidal sea anemone anthopleura elegantissima

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