Pacific Science (1994), vol. 48, no. I: 32-43© 1994 by University of Hawaii Press. All rights reserved

Inorganic Nutrient Fluxes in Anemone-dominated Tide Pools!

SUSAN L. JENSEN2 ,3 AND GISELE MULLER-PARKER2,4

ABSTRACT: Physical and chemical characteristics of seawater in two naturaltide pools on Rosario Beach, Fidalgo Island, Washington, were comparedduring midday low tides in July 1991. One pool contained a mixed assemblageof macroalgae (40% cover) and invertebrates (50% cover). The second pool wasdominated (75% cover) by the sea anemone Anthopleura elegantissima (Brandt,1835), which contains symbiotic algae (zooxanthellae). Temperature, salinity,dissolved oxygen, and pH levels increased in both pools with irradiance andlength of emersion. The resident organisms caused changes in the inorganicnutrient levels of the tide-pool seawater. Anthopleura elegantissima releasedsubstantial amounts of ammonium; NH4 + in the anemone-dominated poolincreased by 33% whereas NH4 + declined in the mixed assemblage pool by anaverage of 28%. Nitrate and nitrite declined in both pools, whereas phosphateremained constant during the 6-hr sampling periods. NH4 + release by A.elegantissima was confirmed in studies of artificial tide pools, where NH4 + levelsincreased by an average of 71 % over an 8-hr period. Release of ammonium byA. elegantissima under natural conditions in the field provides a contrast tonutrient fluxes observed for tropical symbiotic associations.

THE TIDE POOL IS a dynamic ecosystem, chang­ing with the ebb and flow of the tides. At hightide the pools are submerged, the water iscontinuously exchanged, and the system re­mains open. When the tide recedes, the tidepool is suddenly isolated and becomes aclosed ecosystem for different periods of time.Although tide-pool organisms remain in anaquatic environment during low tides, theymay be subjected to large temperature andsalinity changes, as well as fluctuations indissolved inorganic materials such as ammo­nium, nitrate, nitrite, phosphate, and oxygen(Klugh 1924, Ganning 1971). The physical

I This research was funded by an NSF REU Site award(OCE-9000676) to Shannon Point Marine Center and byOCE-8996242 to a.M.p. Manuscript accepted 7 Decem­ber 1992.

2 Shannon Point Marine Center, Western WashingtonUniversity, 1900 Shannon Point Road, Anacortes, Wash­ington 98221.

3 Current address: Department of Biology, Universityof South Florida, Tampa, Florida 33620-5150.

4 Author to whom requests for reprints should beaddressed.

and chemical changes ofseawater in tide poolsduring emersion periods have been examinedin numerous studies (Stephenson et al. 1934,Newell 1970, Truchot and Duhamel-Jouve1980, Morris and Taylor 1983, Huggett andGriffiths 1986). However, with the excep­tion of study of oxygen and carbon dioxidechanges associated with differences in pri­mary production in animal and algae tidepools (Stephenson et al. 1934), none havetargeted specific tide-pool inhabitants to ex­amine their effect on the seawater in the tidepool. Changes in the inorganic nutrients dur­ing emersion periods may provide new infor­mation about the tide-pool organisms.

Anthopleura elegantissima (Brandt, 1835)is a temperate sea anemone that is abundantin the intertidal zone along the coast ofthe northeastern Pacific Ocean (Hand 1955).These anemones contain photosynthetic sym­biotic algae (zooxantheliae) that are highlyproductive; gross production by A. elegan­tissima is comparable with that of intertidalmacroalgae on an areal basis (Fitt et al. 1982).Tropical and temperate algal-cnidarian sym-

32

Inorganic Nutrient Fluxes in Tide Pools-JENSEN AND MULLER-PARKER 33

bioses differ with respect to the supply ofzooplankton food and the nutrient content ofthe seawater, both of which are much higherin the temperate waters of the northeasternPacific Ocean. Studies of tropical symbioticcorals have shown that inorganic nutrients aretaken up and retained within the symbiosis bythe zooxanthellae (D'Elia 1977, Muscatineand D'Elia 1978, Szmant et al. 1990). Further­more, nitrogen and phosphorus exchangesbetween symbiotic invertebrates and seawaterare related to the feeding history of thehost. WeB-fed hosts release both ammonium(Szmant-Froelich and Pilson 1984) and phos­phate (MuBer-Parker et al. 1990) into theseawater environment as waste products. Incontrast to tropical symbioses, there is noinformation about the nutrient fluxes betweenA. elegantissima and seawater. These sym­biotic anemones, having more availablefood, may feed more frequently than sym­biotic corals, thus releasing more nutrients aswaste metabolites. The effect of A. elegantis­sima on the nutrient changes in the ambientseawater of the tide pool is explored by acomparison of the physical parameters andnutrient fluxes of a mixed-assemblage pooland an anemone-dominated pool, using addi­tional artificial tide pools containing only

A. elegantissima. If feeding by A. elegantis­sima results in a greater release of nutrientsinto the ambient seawater, this shouldbe detected in tide pools containing theseanemones.

MATERIALS AND METHODS

Tide Pools

Two natural rock tide pools at Rosa­rio Beach, Washington, on Fidalgo Island(122°39'50" N, 48°25'14" W) were each sam­pled on three consecutive days in July 1991,during low tides that exposed these poolsduring the midday period. Both pools wereformed by the retention ofseawater in naturaldepressions, and there was no groundwaterinput. Tide pool 1 was selected as a represen­tative pool of the midintertidal zone, becauseit contained a diverse assemblage of macro­algae, invertebrates, and fish. Tide pool 2was chosen for its large number of A. ele­gantissima. Percentage cover by the differentorganisms was assessed by placing a 0.25-m 2

quadrat over the pool and measuring the arealdistribution of dominant classes of organismsas viewed from above the pool. Table I lists

TABLE 1

CHARACTERISTICS OF NATURAL TIDE POOLS AT ROSARIO BEACH, WASHINGTON, DURING JULY 1991

CHARACTERISTICS

Pool area (m)Pool volume (liters)Tidal height 1ft (m)]Species present (% cover)

Macroalgae

Invertebrates

Vertebrates

TIDE POOL 1

1.6 by 2.1432.3 (0.7)

(40%)Fucus gardneri SilvaLealhesia difformis (Linnaeus) AreschougVim sp.Endocladia muricala (Postels & Ruprecht)

Agardh

A. eleganlissima (25%)Balanus glandula Darwin (15%)Pagurus hirsuliusculus (Dana)Hemigrapsus nudus (Dana)Collisella pella (Rathke) (10%)

Oligocotlus maculosus Girard (sculpin)

TIDE POOL 2

1.3 by I305.1 (1.55)

«1%)Cladophora sp.

A. eleganlissima (75%)Balanus glandula (10%)Litlorina sp. (2.5%)Nucella emarginata (Deshayes) (2.5%)Collisella pella (10%)

34

the physical characteristics and the residentorganisms of each tide pool. A third set ofartificial tide pools containing only A. ele­gantissima was sampled on 2 days in August1991. The artificial tide pools were round (40cm diam.), shallow, plastic bowls that held 3.8liters of seawater. Sixty-four anemones wereplaced into each of two artificial tide pools.Anemones for the artificial tide pools werecollected on 3 August 1991 at Skyline Beach,Anacortes, Washington, at an approximatetidal height of 1.5 ft. (0.46 m). A third artificialtide pool containing only seawater (4.6 liters)served as a control. The artificial tide poolswere exposed to unshaded natural light out­side and were sampled on 7 and 10 August1991. Between days of sampling, pools werekept submerged in a flow-through seawatersystem at ambient temperature (12°C).

Data Collection

Tidal heights of pools were establishedusing a surveying level, a stadia rod, and areference tidal height at the water's edge.Temperature, salinity, dissolved oxygen, andirradiance were measured in situ at one site inthe middle ofeach tide pool. Temperature wasmeasured with a mercury thermometer, salin­ity with a temperature-compensated refrac­tometer (Reichert-Jung, Cambridge Instru­ments, Buffalo, New York), and dissolvedoxygen with an oxygen probe (Model 57,Yellow Springs Instr. Co., Yellow Springs,Ohio) and meter. Irradiance was measuredwith a 4n underwater quantum sensor con­nected to a datalogger (LI-1000, LI-COR,Inc., Lincoln, Nebraska); irradiance dataaveraged over 15-min intervals were subse­quently downloaded to a computer. Nutrientconcentrations within the tide pools weremonitored by taking seawater samples fromthe tide pools with an acid-washed 30-mlsyringe and filtering the sample through aGFJF (Whatman International, Maidstone,England) filter (nominal pore size 0.7 11m) heldin a Gelman (Gelman Sciences Inc., AnnArbor, Michigan) filter holder. Filtered watersamples were placed in acid-washed polyeth­ylene bottles and kept on ice until broughtback to the laboratory (within 2-7 hr). Sea-

PACIFIC SCIENCE, Volume 48, January 1994

water samples were also collected from theocean for comparison with tide-pool samples.At the laboratory, 10 ml was removed fromeach sample for determination ofpH (Parsonset al. 1984), and the remainder was frozen at- 15°C. Samples were thawed immediatelybefore analysis of nutrients.

The samples were analyzed for ammonium(NH4 +) by the phenol-hypochlorite methodand phosphate (P043-) as specified in Parsonset al. (1984). Both analyses were scaled for a5-ml sample size, and absorbance of the finalproducts was measured on a diode arrayspectrophotometer (Hewlett-Packard 8452).Combined nitrate and nitrite of samples wasmeasured with an autoanalyzer using a cad­mium reduction column (Parsons et al. 1984)and an autoanalyzer (ALPKEM RFA 300,Perstorp Analytical, Wilsonville, Oregon)(RFA method: nitrate + nitrite-nitrogen, no.A303-SI70).

The artificial pools were placed at groundlevel outdoors in an unshaded area protectedfrom the wind near the laboratory at the startof each sampling period. The pools weresampled during the same time of day as thenatural pools, but there was no delay betweenremoval of the pools from the flow-throughseawater system and the first pool measure­ments. All sampling procedures were similar,except that the pH was measured immediatelyafter collection, and the water samples werefrozen within 10 min of collection. Irradiancewas measured in the control pool and wasassumed to be the same for all three pools.Salinity, temperature, and dissolved oxygenwere measured in each of the three pools.

RESULTS

Tide Pool]

Tide pool I (see Table I) was isolated fromthe ocean for 3 hr, 20 min; 3 hr, 10 min; and2 hr, 50 min, respectively, on 10, II, and 12July before sampling began. Temperature in­creased linearly from 14°C to a maximumvalue of 31°C at 1500 hr on 12 July, andsalinity rose from 29 to 31 %0. Underwater

f . § gPM b?8 i i2Lt2liiJ!J2Z!i 1&1 !4

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1200 1400· 1600

Time of day (h)

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16001400120010000800O+----...-----,----.--.,.--...---"T---r--.,.--.....--,---.

0600

Time of day (h)FIGURE I. Irradiance in the natural and the artificial tide pools at Rosario Beach, Washington, 1991: (a) Natural tide

pools. Tide pool I data are connected by solid lines and tide pool 2 data by dotted lines. Pool I was sampled II(e) and 12 July (t.). Light data for pool I on 10 July are missing. Pool 2 was sampled 22 (A), 23 (D), and 24 July(.). (b) Artificial tide pools. Light data collected 7 August are connected by the solid line (0) and light data from 10August by the dotted line (e).

a pool 1

20c(])

(J) 16~xo

"U 12(])'.> Eo 8Cf)Cf).-o 4

.<0'.... ,.....•...•.:::tj ..............~ ....

.i!I-.'::.~~:: ..O·0'.' u

o'

••

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pool 2

oceanv

1400120010000800O+---..---.---......---.---....---.---....---r--....---r-----.0600

Time of day (h)

b 12

c(])CJ)>.xo"U(])

>oeneno

10

8

""--0

160014001200100008006+---..---.---......---.---......---.---......---.---....---.------.0600

Time of day (h)

FIGURE 2. Dissolved oxygen in the natural and the artificial tide pools at Rosario Beach, Washington, 1991:(a) Natural tide pools. Tide pool I data are connected by solid lines and tide pool 2 data by dotted lines. Pool I wassampled 10 (0), II (e), and 12 July (d). Pool 2 was sampled 22 Ct.), 23 (D), and 24 July (.). Dissolved oxygenconcentration of the adjacent ocean is indicated by the v symbol (± SE, obscured by symbol). (b) Artificial tidepools. Data collected 7 August are connected by the solid lines and data from 10 August by the dotted lines. PoolA (0) and pool B (e) contained 64 A. elegantissima each; the control pool data for each date are indicated by thelines without symbols.

M¥¥ A"1

Inorganic Nutrient Fluxes in Tide PoolS-JENSEN AND MULLER-PARKER 37

irradiance increased from 50 to 1600 J.lmolphotons' m- 2

. sec-1 (Figure la). Dissolvedoxygen increased from 8 mg/liter to supersat­urated concentrations (Figure 2a) that werealso noted by the presence of oxygen bubbles.The pH increased an average of 1.08 unitsover the 7-hr time course of measurements,from an initial value of 7.5 to 8.6. Dissolvedinorganic nitrogen levels declined in the tidepool during the day. Ammonium levels drop­ped from 1.8 to 1.0 J.lM, but remained close toconcentrations determined for the adjacentocean seawater (Figure 3a). Combinednitrate and nitrite levels also decreased withtime on each of the 3 days (Figure 4a).Phosphate levels were variable and decreasedonly slightly, the largest change taking placeon II July, from 2.4 to 1.7 J.lM (Figure 5a).

Tide Pool 2

Sampling began 4 hr, 30 min; 4 hr, 5 min;and 3 hr, 35 min after the pool was isolatedby the ebb tide on 22, 23, and 24 July,respectively. Temperature rose from 13°C tothe maximum value of 26°C at 1300 hr on 23July, and salinity and underwater irradiance(Figure la) increased as in the first pool,except for 24 July, which was a cloudy day(Figure la). Dissolved oxygen increased withirradiance, but the increase was more gradualthan in tide pool I, going from 2.2 mg/liter tonear seawater levels by 1300 hr (Figure 2a).Initial pH values were low (pH = 6.9) relativeto that of the ocean (pH = 7.3). The pH didnot exceed 7.5 at any other time. In contrastto tide pool I, levels of both ammonium andphosphate increased with time. Ammoniumconcentrations in tide pool 2 were an order ofmagnitude greater than that of the adjacentseawater, starting at 12.2 J.lM and attaining18.3 J.lM on 24 July (Figure 3a). Phosphatelevels were also higher in the tide pool. Phos­phate increased from an initial concentrationof 3.6 J.lM to 6.5 J.lM on 24 July (Figure 5a).Nitrate and nitrite concentrations were higherthan those obtained in tide pool I and in theadjacent seawater (Figure 4a), although therewas a similar decline in both pools during thesampling period.

Artificial Tide Pools

The differences in the nutrient fluxes ob­served in the two natural tide pools suggestedthat the anemones in tide pool 2 releasedconsiderable quantities of dissolved inorganicnutrients (NH4 + and P04

3 -). To test theeffect of A. elegantissima on seawater nutrientlevels, two artificial tide pools (A and B) withanemones as the sole inhabitants were com­pared with a control artificial pool containingonly unfiltered seawater. The artificial tidepools showed trends similar to those of thetwo natural tide pools with respect to temper­ature and salinity. However, physical condi­tions were very different during this set ofexperiments because the sky was continuallyovercast; irradiance in the artificial tide poolsdid not exceed 700 J.lmol· m- 2

. sec-1 (Fig­ure Ib), and the water temperature peakedat 26°C. Salinity levels remained constant(30%0), presumably because oflower tempera­tures and little exposure to wind at the sam­pling site. Dissolved oxygen levels rose onboth days; on 7 August it reached a maximumof 10 mg/liter at 1000 hr in the two anemonepools before decreasing, whereas on 10 Au­gust oxygen levels continued to rise through­out the day, reaching 10 mg/liter in the anem­one pools, but remaining constant in thecontrol pool (Figure 2b). The pH level in­creased slightly (from 7.16 to 7.81 in pool A,7 August), but tended to fluctuate ratherthan increase steadily. Nutrient concentra­tions confirmed that the high level of NH4 +

observed in tide pool 2 was due to the presenceof the anemones. NH4 + increased in the artifi­cial pools containing the anemones, reachinghigher levels on the first sampling date (froman initial 0.7 J.lM to a final 11.4 J.lM in poolA) and increasing more rapidly on 7 Augustthan on 10 August (0.9 to 3.2 J.lM, Figure 3b).Ammonium levels in the control pool re­mained constant. Phosphate showed little, ifany, increase, fluctuating within the range of2.0 to 3.0 J.lM on both days (Figure 5b).Phosphate levels in the control pool remainedconstant on 7 August and rose slightly on 10August. Seawater concentrations of nitrateand nitrite remained constant in the control

..,. pool 2.'.. ' 0·:::·6, .....0•... [1' .

.•...... .•... n.: .. · li1 ::···

..... : .. :r·o'

pool 1ocean

.Gil -aD .000gO • A V-~-~

a 20

16

E::l 12c

~0

E::t

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«4

00600

o~

0800 1000 1200 1400

b12

E::lC 80~

E ::lE«

4

Time of day (h)

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0/ • • ..0

0/ _......e00··· ... 0 ····

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0600 0800 1000 1200 1400

Time of day (h)

FIGURE 3. Seawater ammonium concentrations in the natural and the artificial tide pools at Rosario Beach,Washington, 1991: (0) Natural tide pools. Tide pool I data are connected by solid lines and tide pool 2 data by dottedlines. Pool I was sampled 10 (0), II (e), and 12 July (d). Pool 2 was sampled 22 (...), 23 (D), and 24 July (.).Seawater ammonium is indicated by the v symbol (± SE, obscured by symbol). (b) Artificial tide pools. Datacollected 7 August are connected by the solid lines and data from 10 August by the dotted lines. Pool A (0) andpool B (e) contained 64 A. elegontissimo each; the control pool data for each date are indicated by the lines withoutsymbols.

#!Ii" SA "

."." ..o .•.

····O··::·O···~: .. ··,. . .....•...···o .. :::·~~:.... pool 2

···0 .... ·0

a 3.0

Q)2.5

+-''C+-' 2.0.-c

+ ~::.t 1.5

Q)+-'C~ 1.0~Z

0.5

0.00600 0800 1000 1200 1400

ocean

Iv1

TIme of day (h)

b 3.0

Q)+-''C~ 2.5c+~Q)

+-'C~ 2.0~Z

Co" " :8:-:-:-:':':': ~ ~ ~ ~ ~6':':':':':'~:::::: ~':::::.•0 .. · .. ·0·· .. ··0

14001200100008001.5 +---.,..---y---r---r----.---,--........--,----.----,----.

0600

TIme of day (h)

FIGURE 4. Seawater combined nitrate and nitrite concentrations in the natural and the artificial tide pools atRosario Beach, Washington, 1991: (a) Natural tide pools. Tide pool I data are connected by solid lines and tide pool2 data by dotted lines. Pool I was sampled 10 (0), II (e), and 12 July (a). Pool 2 was sampled 22 (.), 23 (0), and24 July (.). Seawater concentrations are indicated by the v symbol (± SE). (b) Artificial tide pools. Data collected7 August are connected by the solid lines and data from 10 August by the dotted lines. Pool A (0) and pool B (e)contained 64 A. elegantissima each; the control pool data for each date are indicated by the lines without symbols.

....

pool 1

O~-==-~~~/~._.-- --....

•:: o:::::~·····D

0,:···0' .• •'. ....

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oceanv

pool 2

1400120010000800

a 8

7

6Q)

+J 50-C ~

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00600

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14001200100008001.5 +--.........--r------.-----r---.---r---.---~-.........-___,r_--.

0600

Time of day' (h)

FIGURE 5. Seawater phosphate concentrations in the natural and the artificial tide pools at Rosario Beach,Washington, 1991: (a) Natural tide pools. Tide pool I data are connected by solid lines and tide pool 2 data by dottedlines. Pool I was sampled 10 (0), II (e), and 12 July (...). Pool 2 was sampled 22 (.~), 23 (0), and 24 July (.).Seawater concentrations are indicated by the v symbol (± SE, obscured by symbol). (b) Artificial tide pools.Data collected 7 August are connected by the solid lines and data from 10 August by the dotted lines. Pool A (0)and pool B (e) contained 64 A. elegantissima each; the control pool data for each date are indicated by the lineswithout symbols.

"IMR gaiM

Inorganic Nutrient Fluxes in Tide Pools-JENSEN AND MULLER-PARKER 41

pool and in the two pools with A. elegantis­sima (Figure 4b).

DISCUSSION

The changes in the inorganic nutrient con­centrations in the two natural tide pools arerelated to the differences in the species compo­sition of each pool. The seawater in tide pool1, which contained substantial algal cover(Table I), showed the influence of algal activ­ity overriding that of the resident animals inthe following ways. High rates of primaryproductivity related to increased irradianceduring midday emersion resulted in highlevels of dissolved oxygen and high pH. Theconcentration of dissolved inorganic nitrogendecreased with time, indicating net algal nutri­ent uptake of the nutrients produced as meta­bolites by the animal population. In contrast,the biological and chemical characteristics ofa tide pool dominated by animal biomass (tidepool 2) include a slower rate of oxygen evolu­tion with increase in irradiance (Figure 2a),low pH, and high ammonium output (Figure3a).

Physical Factors

The temperature and salinity data obtainedfor the two natural pools confirm results fromprevious studies of isolated tide pools (Gan­ning 1971, Morris and Taylor 1983, Huggettand Griffiths 1986). Klugh (1924) stressedthe importance of temperature as a limitingfactor; salinity was emphasized by Newell(1970), and Ganning (cited in Newell [1970])found that organisms commonly inhabitingtide pools can tolerate large fluctuationsof salinity. In our study salinity increasedonly slightly (1.3%0), whereas temperatureincreased an average of 10oe, suggesting thattemperature may be the main physical factoraffecting the distribution of tide pool organ­isms during the midday low tides. It is impor­tant to note that these midday low tides occuronly during the summer. During winter, lowtides occur during the night. Therefore, thephysical parameters measured in this studyrepresent extreme highs for this local area.

Dissolved Oxygen

The rapid rise in levels of dissolved oxygenin tide pool I was caused by photosynthesisby the large population of macroalgae (TableI). In tide pool 2, the increase in dissolvedoxygen indicated net production by the smallclump of the macroalga Cladophora and themicroalgae, including the symbiotic algae inthe anemones (Figure 2a). The early morninglow tides left the tide pools isolated for up toseveral hours in the dark before sampling.The high animal biomass in tide pool 2 ex­plains the low initial oxygen concentrationsand pH. During the dark period animal respi­ration depletes oxygen in tide pools (Truchotand Duhamel-Jouve 1980), and increasesin carbon dioxide concentration from ani­mal respiration result in low pH of seawater(Truchot and Duhamel-Jouve 1980, Morrisand Taylor 1983). It is also possible that thehigh NH4 + in tide pool 2 contributed to thelow pH.

Inorganic Nutrients

The most interesting comparison betweenthe tide pools is the change in the inorganicnutrients within each tide pool. Tide pool Ishowed a decrease in ammonium concentra­tion (Figure 3a); presumably this nutrient wasbeing taken up by the algae during photosyn­thesis. In the same pool, nitrate and nitritelevels decreased slightly (Figure 4a), as didthat of phosphate (Figure Sa). The resultsfrom tide pool 2 were completely different:ammonium increased to very high concentra­tions, and phosphate levels also increased(Figures 3a and Sa). This occurred in spite ofthe fact that the dominant animal resident ofthe tide pool was the symbiotic anemoneA. elegantissima, whose zooxanthellae are ex­pected to retain nutrients, especially in thelight. Zamer and Shick (1987) found that theNH4 + excretion rate of algae-free A. ele­gantissima was greater than that of symbioticA. elegantissima in the dark, indicating thatsome retention ofNH4 + by the zooxanthellaemay take place in this anemone. Even ifNH4 +

is retained by A. elegantissima, our resultsshow that an excess is released at all times. The

42

increase in phosphate in tide pool 2 may be aproduct of anemone metabolism, as previ­ously shown by Muller-Parker et al. (1990)with Aiptasiapallida (Verrill), but the artificialtide pools containing only A. elegantissimashowed little change in phosphate levels (Fig­ure 5b), indicating that the phosphate increasein tide pool2 must have been from some othersource. The decrease in nitrate and nitritelevels in tide pool 2 was not caused by uptakeby the anemones, based on the lack of changein concentration in the artificial tide pools(Figure 4b).

The higher initial concentrations of allnutrients in tide pool 2 may represent meta­bolites released by the anemones, with littlemacroalgae (relative to pool I) to depleteseawater nutrient levels during the day. Sam­pling began in the artificial tide pools immedi­ately after isolation, so initial concentrationsof inorganic nutrients are those of the flow­through seawater system. Ammonium releaseby anemones on 7 August, 4 days after collec­tion, was much higher than that on 10 August,7 days after collection (Figure 3a). The differ­ence in the amount of ammonium producedby the anemones in the artificial tide poolsduring the first and second set of experimentssuggests that maintenance of the anemoneswithout feeding caused a reduction in therelease of ammonium. Ammonium levels intide pool 2 (Figure 3b) showed that anemonesincreased the ammonium in seawater by anorder of magnitude only hours after isolationof the tide pool from the ocean. Rates ofammonium production by symbiotic cnida­rians vary with the host animal's diet: higherprotein intake leads to higher ammoniumoutput (Muscatine 1980, Zamer and Shick1989, Szmant et al. 1990). The increase in theammonium concentration of the seawater intide pool 2 is highly suggestive that theseanemones had fed recently on N-rich prey.The results also suggest that A. elegantissimamay be an important source of dissolvedinorganic nitrogen for macroalgae in tidepools.

Our study indicates that nutrients are notconserved by field populations of A. ele­gantissima. Symbiotic associations betweenzooxanthellae and cnidarians are predicted to

PACIFIC SCIENCE, Volume 48, January 1994

retain inorganic nutrients because the algaerequire these for growth (Muscatine 1980).Our work with tide pool anemone popula­tions suggests that nutrient cycling betweensymbiotic algae and their animal hosts is nottightly coupled in temperate symbioses suchas the A. elegantissima association. This pro­vides a sharp contrast to zooxanthellae intropical symbioses where inorganic nutrientsupplies and prey are scarce. The differencesbetween temperate and tropical symbioticassociations merit further investigation.

ACKNOWLEDGMENTS

We thank A. Summers for assistance withthe field sampling.

LITERATURE CITED

D'EuA, C. F. 1977. The uptake and releaseof dissolved phosphorus by reef corals.Limnoi. Oceanogr. 22:301-315.

FlIT, W. K., R. L. PARDY, and M. M.LITTLER. 1982. Photosynthesis, respiration,and contribution to community produc­tivity of the symbiotic sea anemone An­thopleura elegantissima (Brandt, 1835). J.Exp. Mar. BioI. Ecoi. 61 :213-232.

GANNING, B. 1971. Studies on chemical, phys­ical and biological conditions in Swedishrockpool ecosystems. Ophelia 9: 51-105.

HAND, C. 1955. The sea anemones of CentralCalifornia. Part II. The endomyrian andmesomyrian anemones. Wasmann J. BioI.13:37-99.

HUGGETT, J., and C. L. GRIffiTHS. 1986. Somerelationships between elevation, physico­chemical variables and biota of intertidalrockpools. Mar. Ecoi. Prog. Ser. 29: 189­197.

KLUGH, A. B. 1924. Factors controlling thebiota of tide-pools. Ecology 5: 192-196.

MORRIS, S., and A. C. TAYLOR. 1983. Diurnaland seasonal variation in physico-chemicalconditions within intertidal rock pools.Estuarine Coastal Shelf Sci. 17: 339-355.

MULLER-PARKER, G., C. B. COOK, and C. F.

iii

Inorganic Nutrient Fluxes in Tide Pools-JENSEN AND MULLER-PARKER 43

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