www.elsevier.com/locate/jembe

Journal of Experimental Marine Biolo

Contrasting contributions to inorganic nutrient recycling by the

co-occurring jellyfishes, Catostylus mosaicus and Phyllorhiza

punctata (Scyphozoa, Rhizostomeae)

K.A. Pitta,*, K. Koopb, D. Rissikc

aCentre for Aquatic Processes and Pollution and School of Environmental and Applied Sciences, Griffith University, PMB 50,

Gold Coast Mail Centre QLD 9726, AustraliabEnvironment and Conservation Science, NSW Department of Environment and Conservation, PO Box A290,

Sydney South NSW 1232, AustraliacDepartment of Infrastructure, Planning and Natural Resources, 33 Bridge Street, Sydney NSW 2000, Australia

Received 14 May 2004; received in revised form 1 August 2004; accepted 1 September 2004

Abstract

The rhizostome jellyfishes, Catostylus mosaicus and Phyllorhiza punctata abound in estuaries in New South Wales,

Australia. P. punctata contains symbiotic zooxanthellae but C. mosaicus contains few or no zooxanthellae. Our experiment

measured the rates at which NH3, PO4 and NOx were taken up or excreted by each species and in two controls: a bwater onlyQcontrol and a bmucusQ control. Rates of uptake or excretion were measured as changes in the nutrient concentration of the water

in the containers housing the animals over periods of 6 h. Experiments were repeated twice during the day and twice at night,

under both ambient and enriched nutrient conditions. Under ambient nutrient conditions, the flux of NH3 in the P. punctata

treatment did not differ from the controls but under enriched conditions P. punctata excreted NH3 during the night (49 Ag kg�1

WW (wet weight) h�1) and took up NH3 during the day (123 Ag kg�1 WW h�1). In contrast, C. mosaicus excreted NH3 at a rate

of 1555 Ag kg�1 WW h�1 during the day and 1004 Ag kg�1 WW h�1 during the night under both enriched and ambient nutrient

conditions. P. punctata neither took up nor excreted PO4 but C. mosaicus excreted PO4 at a faster rate during the day than night

(173 Ag kg�1 WW h�1 cf. 104 Ag kg�1 WW h�1). Both C. mosaicus and P. punctata excreted NOx and, although the rate of

excretion for P. punctata varied between the two experiments conducted during the day, the rate of excretion was consistently

greater than for C. mosaicus (52 and 80 Ag kg�1 WW h�1 cf. 26 Ag kg�1 WW h�1). Tubs containing P. punctata had a much

greater concentration of dissolved oxygen at the end of the experiments conducted during the day (152% saturation) than night

(60% saturation) but tubs containing C. mosaicus had a greater dissolved oxygen concentration during the night (47%

saturation) than day (39%). Overall, C. mosaicus appears to recycle more inorganic nutrients to estuaries than P. punctata.

Calculations of the importance of inorganic nitrogen excreted by this species during times of peak biomass in Lake Illawarra

suggest that it can meet about 8% of the phytoplankton primary production requirements of N and that its inorganic N excretion

0022-0981/$ - s

doi:10.1016/j.jem

* Correspon

E-mail addr

gy and Ecology 315 (2005) 71–86

ee front matter D 2004 Elsevier B.V. All rights reserved.

be.2004.09.007

ding author. Tel.: +61 7 5552 8324; fax: +61 7 5552 8064.

ess: K.Pitt@griffith.edu.au (K.A. Pitt).

K.A. Pitt et al. / J. Exp. Mar. Biol. Ecol. 315 (2005) 71–8672

rate is about 11% of measured inorganic ammonia fluxes from sediments in that system. Since the biomass of C. mosaicus often

exceeds several thousand tonnes, the contribution of inorganic nutrients by this species is substantial.

D 2004 Elsevier B.V. All rights reserved.

Keywords: Gelatinous zooplankton; Excretion; Symbioses; Zooxanthellae

1. Introduction

Excretion of inorganic nutrients by consumers is a

major source of recycled nutrients for primary

producers (e.g., Uthicke, 2001; Priddle et al., 2003;

Reissig et al., 2003). Gelatinous zooplankters are

important consumers in pelagic systems where they

frequently represent a large fraction of the biomass

(e.g., Pages et al., 1996, 2001). Because these

consumers occur in such large biomasses, gelatinous

zooplankters are likely to be one of the largest

contributors of recycled nutrients in these areas.

Indeed, in the North Atlantic, excretion by gelatinous

zooplankters has been estimated to supply 39–63% of

the nitrogen required to sustain phytoplankton pro-

duction (Biggs, 1977).

Scyphozoan jellyfish are the most abundant gelat-

inous zooplankters in estuaries in eastern Australia.

Population blooms occur periodically, with abundan-

ces increasing up to 30-fold over periods of just weeks

to months (Pitt and Kingsford, 2000). During such

blooms, the biomass of jellyfish can measure thou-

sands of tonnes (Pitt and Kingsford, 2003) and the

medusae are likely to recycle enormous quantities of

inorganic nutrients to the water column. Scyphozoan

jellyfish differ from most gelatinous zooplankters in

that some species contain symbiotic dinoflagellates

(zooxanthellae) within their tissues (Balderston and

Claus, 1969). Jellyfish with symbiotic zooxanthellae

are likely to recycle fewer nutrients to the water

column since their symbionts may utilise the excre-

tory products of their host (Wilkerson and Kremer,

1992). Jellyfish with and without zooxanthellae (or

with different densities of zooxanthellae) are, there-

fore, likely to have contrasting roles in nutrient

recycling (Cates and McLaughlin, 1976; Muscatine

and Marian, 1982).

Catostylus mosaicus and Phyllorhiza punctata are

large, rhizostome medusae that occur abundantly in

estuaries and coastal lagoons in eastern Australia (Pitt

and Kingsford, 2000). Recent molecular studies show

that both species contain zooxanthellae (Moore,

personal communication), but a recent flurometric

study of the two species failed to detect any photo-

synthesis by C. mosaicus (Hill, personal communica-

tion). Hence, these species are likely to make

contrasting contributions to nutrient recycling in

estuaries.

The aim of our study was to compare rates of

uptake or excretion of the inorganic nutrients ammo-

nia (NH3), nitrate and nitrite (NOx) and phosphate

(PO4) by C. mosaicus and P. punctata. Specifically

we predicted that C. mosaicus would excrete inor-

ganic nutrients but P. punctata would actively deplete

inorganic nutrients from the surrounding water. Since

photosynthesis occurs only during daylight, rates of

nutrient uptake may vary diurnally. Hence we also

tested the hypothesis that the rate of nutrient uptake by

P. punctata would be faster during the day than during

the night while the rate of nutrient excretion by C.

mosaicus would be similar during both day and night.

2. Methods

The study was conducted during February 2003 at

Smiths Lake, an intermittently open coastal lagoon in

New South Wales, Australia. Like most coastal

lagoons in the region, Smiths Lake often contains

dense populations of C. mosaicus and P. punctata

(Pitt, personal observation).

2.1. Experimental treatments

Experiments were repeated twice during the day

(19 and 22/2/2003) and twice at night (18 and 20/2/

2003) to compare rates of nutrient flux when medusae

were and were not photosynthesising. Rates of

nutrient flux were measured for C. mosaicus, P.

punctata and two controls. The first control consisted

K.A. Pitt et al. / J. Exp. Mar. Biol. Ecol. 315 (2005) 71–86 73

of filtered estuarine water and was used to control for

possible variation in nutrient concentrations in the

absence of jellyfish. The second control was termed

the bmucusQ control. Observations showed that, unlikeP. punctata, C. mosaicus produces strings of mucus.

Decomposition of the mucus could potentially con-

tribute inorganic nutrients to the treatment, independ-

ent of excretion directly from the animal. To control

for the differing rates of mucus production between

species, mucus was collected by placing individual C.

mosiacus in tubs of filtered estuarine water. C.

mosaicus were confined for 1 h, after which the

medusae were discarded but the strings of mucus

retained.

2.2. Preparation of estuarine water

Estuarine water was collected approximately 500

m offshore and stored in clean, plastic tubs prior to

filtering. Water was pre-filtered through 10 and 1 Amnose-bag filters before being vacuum filtered through

glass fibre filters and 0.2 Am membrane filters. Forty

litres of filtered estuarine water was transferred to

each of sixteen 60-L rectangular tubs made of clear

plastic. Since it took approximately 16 h to filter all

the water required for each experiment, a lid was

placed on each tub after it was filled to prevent

evaporation or contamination by rain or other

sources.

2.3. Sampling of water for nutrient analyses

Samples of water for nutrient analyses were

extracted from experimental tubs using a syringe.

Duplicate samples of 25 ml were filtered (0.45 Am)

and stored in clean plastic vials. Samples were

initially stored on ice and then transferred to a clean

freezer at the completion of each experiment. Nutrient

concentrations were determined by flow injection

analysis, ammonia by the automated phenate method,

phosphate by the automated ascorbic acid reduction

method and NOx (nitrite and nitrate) by the automated

cadmium reduction method at the New South Wales

Department of Environment and Conservation Water

Science Laboratories. Nutrient concentrations were

measured within two weeks of the experiment being

completed.

2.4. Experimental procedure

Duplicate samples of water were extracted from

each tub prior to starting each experiment to ensure

that no tubs were contaminated (referred to as Time

0). To increase the ability to detect the active uptake of

nutrients, ammonia (NH3), nitrate and nitrite (NOx)

and phosphate (PO4) were added at random to 8 of the

16 tubs to elevate them to concentrations of approx-

imately 58, 30 and 35 Ag L�1, respectively. These

concentrations reflected the upper limit of the nutrient

concentrations found naturally in the lake (Coade,

personal communication). Duplicate samples of water

were again extracted from all tubs immediately after

the addition of nutrients (Time 1). Two replicates of

each of the four treatments (i.e., C. mosaicus, P.

punctata and the Mucus and Water controls) were

assigned randomly to two tubs containing nutrients

and two tubs to which no nutrients had been added.

Jellyfish were collected from the field using a bucket

immediately prior to each experiment and care was

taken to select animals that were undamaged, were

actively swimming and were of similar sizes. The

average bell diameter (BD) of medusae used in the

experiment was identical for both C. mosaicus and P.

punctata and was 209 mm (S.E.=3.8 C. mosaicus;

S.E.=3.5 P. punctata). The mean weight, however,

differed between species: 2161 g (F103 S.E.) for C.

mosaicus and 1623 g (F162 S.E.) for P. punctata.

One C. mosaicus or one P. punctata was added to

each tub, as appropriate, immediately after the

addition of the nutrients. The mucus controls were

set-up slightly differently because the mucus was

collected by confining one C. mosaicus in each of

four tubs containing filtered seawater for 1 h prior to

the start of the experiment. After 1 h, the jellyfish

were removed and nutrients were added to two of the

tubs at the same time that nutrients were added to the

other treatments. Duplicate samples of water were

extracted from each tub every hour for 6 h (Times 2–

7). The bell diameter and wet weight of each jellyfish

was measured at the end of the experiment to

minimise stress to the animals caused by handling.

During the first day and first night experiments, the

tubs were placed in the water parallel to the shore at a

depth of approximately 20 cm so that the temperature

of the water in the tubs was the same as that in the

lake. During the second night experiment, tubs were

Table 1

Summary of results for the four-factor ANOVAs comparing differences in the average concentrations of NH3, PO4 and NOx between Times 1

and 7 and in dissolved oxygen (DO) concentration measured after Time 7

Variable NH3 NOx PO4 DO

Transformation Nil Ln(x+1) Nil Nil

Cochran’s C 0.24 NS 0.24 NS 0.38** 0.24 NS

Level of significance (a) 0.05 0.05 0.01 0.05

Source of variation DF P P P P F vs

1 DvsN 1 * NS NS * 2

2 Ti (DvsN) 2 NSP ***P NSP **P 12

3 Tr 3 *** *** ***P ***P 7

4 N 1 NS NS NS NS 8

5 DvsN�Tr 3 *** NS ***P ***P 7

6 DvsN�N 1 NS NS NS NS 8

7 Tr�Ti(DvsN) 6 NSP **P NS NS 12

8 N�Ti(DvsN) 2 NSP NSP NSP NSP 12

9 Tr�N 3 *P NSP NS NSP 11

10 DvsN�Tr�N 3 *P NSP NS NSP 11

11 N�Tr�Ti(DvsN) 6 NS NS NSP NS 12

12 Residual 32

Pooled sources 11&12 11&12 7&12 7, 11, 12

DvsN=Day vs. Night, Ti(DvsN)=Time(Day versus Night), Tr=Treatment (C. mosaicus, P. punctata, Mucus control and Water control),

N=Nutrients (ambient and enriched). DF=degrees of freedom, F vs=denominator mean square (if not tested over pooled terms). Some terms

were pooled if they were non-significant at a=0.25 to increase the power of tests. P indicates terms were tested over pooled sources of variation.

*Pb0.05, **Pb0.01, ***Pb0.001, NS=non-significant at a=0.05 or a=0.01 as indicated.

K.A. Pitt et al. / J. Exp. Mar. Biol. Ecol. 315 (2005) 71–8674

placed on the shore since strong winds generated

waves that would have washed lake-water into the

tubs. Torrential rain occurred during the field trip and

Fig. 1. Variation in change in NH3 concentrations (i.e., difference between Ti

the day (white bars) and night (grey bars) under ambient and enriched nutrie

amount of NH3 excreted or taken up (Ag kg�1WWh�1). Positive values indi

lines indicate no difference between treatments (from SNK comparisons). C

by the final daytime experiment, terrestrial run-off had

caused dark, tannin-stained water to accumulate close

to shore. Tubs, therefore, were again placed on the

me 1 and Time 7) among treatments for experiments conducted during

nt conditions. Numbers above the bars indicate the average (F1 S.E.)

cate excretion, negative values indicate uptake of nutrients. Horizontal

=C. mosaicus, P=P. punctata, M=Mucus control, W=Water control.

K.A. Pitt et al. / J. Exp. Mar. Biol. Ecol. 315 (2005) 71–86 75

shore because the dark water surrounding the tubs

may have altered the light regime in the tubs and

confounded comparisons between times.

2.5. Physical conditions

Each hour during the experiments, the water

temperature was measured in three randomly selected

tubs and once in the air and once in the water close to

the edge of the lake. Light intensity (photosyntheti-

cally active radiation: PAR) was measured using a

Licor light meter. The light meter was placed in a tub

Fig. 2. Time series of average (F1 S.E.) excretion or depletion of NH3

control, (.) Water control) during the day and night and under ambient and

prior to start of experiment. Time 1=start of experiment. Times 2–7 repre

of seawater and recorded light levels every 5 min over

the duration of each experiment. At the end of each

experiment, the concentration of dissolved oxygen

was measured in each tub using a Yeo-Kal 612 water

quality probe to determine diurnal variations in

relative rates of photosynthesis (i.e., oxygen produc-

tion) between species. Despite the generally inclement

weather, it only rained during the second day experi-

ment. The 35 mm of rain that fell was recorded using

a measuring cylinder and the final concentrations of

nutrients in the tubs were corrected for dilution

accordingly.

for each treatment ((x) C. mosaicus, (E) P. punctata, (n) Mucus

enriched nutrient conditions. Time 0=ambient nutrient concentration

sent 1-h intervals.

K.A. Pitt et al. / J. Exp. Mar. Biol. Ecol. 315 (2005) 71–8676

2.6. Statistical analyses

Differences between the initial (Time 1) and final

(Time 7) concentrations of NH3, NOx and PO4 and

the dissolved oxygen concentration (measured after

Time 7) were analysed using four-way analyses of

variance (ANOVAs). Since there was almost no

difference in the nutrient concentrations of the

duplicate samples of water, the average of the two

samples was used as the variable. The factors

analysed were: Day vs. Night which was a fixed,

orthogonal factor; Time which had two levels, was

nested within Day vs. Night and was a random

factor, Treatment which had four levels (C. mosai-

cus, P. punctata, Water Control and Mucus Control)

and was a fixed, orthogonal factor and Nutrients

which had two levels (Ambient and Enriched) and

was a fixed, orthogonal factor. The assumption of

homogeneity of variances was tested using a

Cochran’s test prior to doing the ANOVAs. If

variances were heterogeneous and were unable to

be stabilised using transformations, a was reduced to

0.01 to reduce the probability of making a Type I

error (Underwood, 1997). Where possible, the power

of tests was increased by pooling lower-order

interactions that were non-significant at P=0.25

(Underwood, 1997). When the ANOVAs identified

Fig. 3. Variation in change in NOx concentrations (i.e., difference between

during the day and night experiments (white bars=Time 1, grey bars=Time

NOx excreted (Ag kg�1 WW h�1). Details as per Fig. 1.

significant differences, post hoc Student–Newman–

Keuls (SNK) tests were used to identify where the

differences occurred.

3. Results

3.1. Analysis of NH3

Concentrations of NH3 varied among treatments

but for some treatments, patterns differed between day

and night, depending on whether the treatments had

been enriched with nutrients (Table 1). C. mosaicus

excreted more nutrients during the day (mean 1555 Agkg�1 h�1) than night (mean 1004 Ag kg�1 h�1), but

during the day excreted slightly more NH3 under

enriched (1605 Ag kg�1 h�1) rather than ambient

(1505 Ag kg�1 h�1) conditions (Fig. 1). The concen-

tration of NH3 in the tubs containing C. mosaicus

increased linearly indicating that the rate of excretion

was constant during the period of the experiments

(Fig. 2). In contrast, under ambient conditions, there

was no difference in the amount of NH3 excreted by P.

punctata during both the day and night, and changes

in concentrations did not differ to those of the controls

(Fig. 1). Under enriched conditions, however, P.

punctata took up NH3 during the day (123 Ag kg�1

Time 1 and Time 7) among treatments for replicate times sampled

2). Numbers above the bars indicate the average (F1 S.E.) amount of

K.A. Pitt et al. / J. Exp. Mar. Biol. Ecol. 315 (2005) 71–86 77

h�1) and excreted it during the night (49 Ag kg�1 h�1)

(Fig. 1). Although P. punctata did influence the flux

of nutrients under enriched conditions, the amount of

NH3 taken up or excreted by P. punctata was

substantially less than that excreted by C. mosaicus.

Concentrations of NH3 did not vary diurnally or under

ambient or enriched conditions for either the Mucus or

Water controls (Fig. 1).

3.2. NOx

The flux of NOx was much smaller than that of

either NH3 or PO4 (Fig. 3). Concentrations of NOx

Fig. 4. Time series of average (F1 S.E.) excretion or depletion of NOx f

enriched nutrient conditions. Details as per Fig. 2.

varied among treatments but for P. punctata and the

two controls, the concentration of NOx also varied

between the two daytime experiments (Table 1), with

concentrations being greater during the second day-

time experiment (Fig. 3). Rates of excretion of NOx

by C. mosaicus, however, were consistent between

times. During both daytime experiments, the rate of

excretion by C. mosaicus (average 25.5 Ag kg�1 h�1)

was less than that of P. punctata (52 and 80 Ag kg�1

h�1; Fig. 3). Rates of excretion of NOx by P. punctata

were mostly linear under ambient nutrient conditions

indicating a constant rate of excretion, but under

enriched conditions, the rate of uptake appeared to

or each treatment during the day and night and under ambient and

K.A. Pitt et al. / J. Exp. Mar. Biol. Ecol. 315 (2005) 71–8678

slow or stop after Time 5 during the day, but

seemed to accelerate between Times 6 and 7 at night

(Fig. 4).

3.3. PO4

Concentrations of PO4 varied among treatments

but trends were not consistent between day and night

(Table 1). C. mosaicus excreted PO4 at a faster rate

during the day (173 Ag kg�1 h�1) than night (104 Agkg�1 h�1) (Fig. 5) and the linear increase in

concentrations of PO4 again suggested that the rate

of excretion was constant for the duration of the

experiments (Fig. 6). There was no statistical differ-

ence in nutrient flux between P. punctata and either

of the controls, although there was a slight trend for

P. punctata to excrete very small amounts of PO4

(Figs. 5 and 6).

3.4. Physical variables

3.4.1. Irradiance

No light was detected during either of the experi-

ments conducted at night, but there was great variation

in irradiance between the two experiments conducted

Fig. 5. Variation in change in PO4 concentrations (i.e., difference

between Time 1 and Time 7) among treatments for experiments

done during the day (white bars) and night (grey bars). Numbers

above the bars indicate the average (F1 S.E.) amount of PO4

excreted (Ag kg�1 WW h�1). Other details as per Fig. 1.

during the day (Fig. 7). During the first day experi-

ment, there were periods of patchy cloud cover

interspersed with long periods of sunshine. Irradiance

exceeded 500 AE m�2 s�1 for 44% of the time and

exceeded 200 AE m�2 s�1 for 86% of the time. In

contrast, heavy cloud on the second day limited

irradiance to, on average, 92 AE m�2 s�1 for the first

2.5 h of the 6-h experiment and to 111 AE m�2 s�1 for

the last 90 min of the experiment (Fig. 7). Irradiance

exceeded 500 AEm�2 s�1 for only 19% of the time and

exceeded 200 AE m�2 s�1 for only 26% of the time.

3.4.2. Temperature

During the experiments, the temperature of the

water in the tubs ranged between approximately 22

and 28 8C (Fig. 8). Although the tubs were placed on

shore during the second day and night experiments,

the temperature in the tubs was a maximum of only

2–3 8C cooler than the water in the lake.

3.4.3. Concentration of dissolved oxygen

The concentration of dissolved oxygen at the end

of the experiments varied among treatments, but

trends were not consistent between the day and night

experiments (Table 1). Concentrations of dissolved

oxygen were much greater during the day (152%

saturation) than night (60% saturation) for P. punctata

(Fig. 9a). In contrast, concentrations of dissolved

oxygen were greater during the night (47% saturation)

than day (39% saturation) for C. mosaicus (Fig. 9a).

The dissolved oxygen concentrations were similar

between the day and night experiments for both of the

controls, but the dissolved oxygen concentration of

the Water Control was greater than that of the Mucus

Control during both the day and night experiments

(Fig. 9). The percentage saturation of oxygen also

varied among times (Table 1). The concentration of

dissolved oxygen was slightly greater during the

second (20/2/03) night experiment (73%), compared

to the first (18/2/03; 67%; Fig. 9b). There was no

difference in the concentration of dissolved oxygen

between the two experiments done during the day.

4. Discussion

The major objective of our study was to compare

the contributions of C. mosaicus and P. punctata to

Fig. 6. Time series of average (F1 S.E.) excretion or depletion of PO4 for each treatment during the day and night and under ambient and

enriched nutrient conditions. Details as per Fig. 2.

K.A. Pitt et al. / J. Exp. Mar. Biol. Ecol. 315 (2005) 71–86 79

the recycling of inorganic nutrients. The contributions

of the two medusae varied depending upon the nutrient

studied. For NH3, the results were largely as predicted,

with C. mosaicus excreting much greater quantities of

NH3 than P. punctata. For both species, the rates of

excretion varied diurnally and under enriched nutrient

conditions, P. punctata conformed to predictions by

actively taking up NH3 during the day (i.e., when

photosynthesising) and excreting it at night. Variation

in rates of uptake of NH3 by P. punctata under

enriched nutrient concentrations are consistent with

observations that rates of uptake of ammonia by the

coronate scyphozoan, Linuche unguiculata, were

positively correlated with the initial concentration of

NH3 in the experimental container (Wilkerson and

Kremer, 1992). Although P. punctata did actively take

up or excrete NH3 in measurable quantities, rates of

flux were very slow and the magnitude of the fluxes in

the P. punctata treatments were not much greater to

those observed in either the Mucus or Water controls.

Such observations are consistent with the hypothesis

that dense concentrations of zooxanthellae in P.

punctata actively take up NH3, resulting in tight

nutrient cycling and no or minimal net release of NH3

to the water column. Our data, however, cannot

determine whether the symbionts take up NH3 directly

Fig. 7. Temporal variation in irradiance during the two experiments conducted during the day. (x) 19/2/2003; (n) 22/2/2003. No light was

detected during the two night experiments.

K.A. Pitt et al. / J. Exp. Mar. Biol. Ecol. 315 (2005) 71–8680

from the host’s excretory products within the organ-

ism, or indirectly from the water column, subsequent

to it being excreted by P. punctata. To determine the

pathway by which the zooxanthellae take up nutrients,

isotopic labelling experiments need to be done.

Regardless of the mechanism by which zooxanthellae

utilise NH3, the net contribution of P. punctata to

nutrient recycling is almost negligible, whereas C.

mosaicus appears to contribute significant amounts of

NH3 to the surrounding water.

Comparison of rates of uptake or excretion among

taxa are difficult because metabolic rates vary depend-

ing upon the temperatures at which experiments are

done, the nutritional status of the animal at the time of

the experiment and the body mass of the species

studied (Kremer, 1982; Schneider, 1989; Matsakis and

Conover, 1991; Matsakis, 1992). Schneider (1989)

compared weight-specific rates of excretion of ammo-

nia between the semaeostome Aurelia aurita and

various other gelatinous zooplankters by using the

Q10 law to correct for the different temperatures at

which the various studies were done. By converting

rates of excretion to the same units and using the Q10

law (assuming a Q10 value of 2; Ikeda, 1985) to

correct for temperature, rates of excretion of ammonia

of C. mosaicus can also be compared to other species.

Rates of excretion by C. mosaicus were substantially

less than those measured for the semaeostome A.

aurita and several species of ctenophore (Table 2).

Metabolic rates tend to be faster in smaller species,

and because C. mosaicus weighs considerably more

than the other species listed in Table 2, these results

are consistent with the predication by Schneider

(1989) that because of their heavy body mass and

consequently their smaller surface area to volume

ratio, large scyphomedusae would have considerably

slower rates of excretion than smaller gelatinous

species.

In contrast to the patterns observed for NH3, P.

punctata consistently recycled twice as much NOx as

C. mosaicus, even though the amount excreted by P.

punctata varied between the two daytime experiments

and the absolute amounts of NOx–N was much

smaller than NH3–N. These observations indicated

that NOx was not being utilised by the zooxanthellae

in P. punctata. Studies of the flux of nitrate by

symbiotic marine cnidarians have produced mixed

results. Some species actively take up nitrate, but

others do not (Miller and Yellowlees, 1989). The

observation that P. punctata did not actively take up

NOx is consistent with studies that indicate that NH3

is taken up preferentially to nitrate and that nitrate

may be actively excreted by zooxanthellate medusae

(e.g., Muscatine and Marian, 1982). Compared to the

rate of excretion of NH3 by C. mosaicus, rates of

excretion of NOx by both species were small and NH3

Fig. 8. Time series of temperatures measured in the lake, air (20 and 22/2/03 only) and average (F1 S.E.) of water temperatures measured in

three tubs during each experiment.

K.A. Pitt et al. / J. Exp. Mar. Biol. Ecol. 315 (2005) 71–86 81

appears to be the major contributor to nitrogen

recycling.

Despite large differences in irradiance between the

two daytime experiments, P. punctata produced

similar quantities of O2 during both days and, with

the exception of NOx, also excreted or took up similar

amounts of nutrients. Our measurements of oxygen

production were crude because tubs were not sealed

and oxygen would have been exchanged with the

atmosphere. Although this prevented us measuring

absolute rates of photosynthesis, it still enabled the

relative rates of photosynthesis between experiments

to be compared. The production of similar amounts of

oxygen by P. punctata during both day experiments

indicates that the rate of photosynthesis of zooxan-

thellae within P. punctata was similar between days,

despite the differences in irradiance. For this to occur,

the saturation irradiance of P. punctata must have

been equal to or less than the lower range of the

irradiance observed during the second daytime experi-

ment. The saturation irradiance has been measured for

only a few species of zooxanthellate jellyfish but for

those studied, it varies between 134 AE m�2 s�1 for

the lake ecotype of Mastigias papua (McCloskey et

al., 1994) and 414 AE m�2 s�1 for Cassiopea

xamachana (Verde and McCloskey, 1998). In our

study, irradiance exceeded 200 AE m�2 s�1 for 86% of

the first and only 26% of the second daytime

experiments yet rates of photosynthesis remained

similar. This suggests that the saturation irradiance

Fig. 9. Variation in percentage saturation of dissolved oxygen (a) among treatments during the day (white bars) and night (grey bars) and (b)

between replicate experiments conducted during the day and night). C=C. mosaicus, P=P. punctata, M=Mucus control, W=Water control.

K.A. Pitt et al. / J. Exp. Mar. Biol. Ecol. 315 (2005) 71–8682

for P. punctata is less than 200 AE m�2 s�1 and may

more closely resemble that of M. papua than C.

xamachana. The photophysiology of C. mosaicus and

P. punctata is being investigated in a separate study

(Pitt and Hill, unpublished data).

Rates of excretion are correlated with temperature.

For example, (Matsakis, 1992) observed that excretion

of ammonia by the hydromedusa Clytia sp. increased

with increasing temperature, although the nature of the

relationship varied depending on the availability of

food. Weather conditions prevented the second day

and night experiments from being conducted in situ

and for these experiments the temperatures of the

experimental tubs were 2–3 8C cooler than the lake

water. This may have caused excretion rates to be

slower. The only difference detected between replicate

day and night experiments, however, was that P.

punctata excreted more NOx during the second

Table 2

Weight-specific measurements of rates of excretion of ammonia (Amol NH4-Ng-1 WW day-1) by scyphozoan medusae and ctenophores

Species Original data T (8C) Data corrected for 15 8C n Source

C. mosaicus 0.85–2.23 25 0.425–1.11 16 This study

Aurelia aurita 29–94 15.0 29–94 23 (Schneider, 1989)

Mnemiopsis leidyi 10–36 10.3–24.5 10–18 6 (Kremer, 1977)

Mnemiopsis mccradyi 10–42 22.0 6–26 4 (Kremer, 1982)

Beroe sp. 9.5 �0.8 28.3 1 (Ikeda and Mitchell, 1982)

WW=wet weight, n=number of replicates. Table adapted from (Schneider, 1989). Data were corrected for temperature using the Q10 law

(Ikeda, 1985).

K.A. Pitt et al. / J. Exp. Mar. Biol. Ecol. 315 (2005) 71–86 83

daytime experiment and these results are inconsistent

with the cooler temperature during the second daytime

experiment reducing the metabolic rate of the medu-

sae. Hence, it appears that the different temperatures

experienced between replicate day and night experi-

ments were not sufficient to cause detectable changes

in rates of excretion.

A potential confounding factor in our experiment

was that the zooplankters captured on the oral arms of

the medusae were not removed prior to the experi-

ments and so some of the nutrients released into the

tubs may have been derived from decomposition of

the medusae’s prey rather than excretion. We made a

conscious decision not to remove the prey as it would

have required either confining the jellyfish for periods

of several hours in filtered water (to allow the prey to

be digested) or vigorously washing the oral arms to

remove the prey. Either of these procedures would

have increased the stress on the animals and, there-

fore, had the potential to influence their metabolic

rates. The consequences of retaining the zooplankton

were that it would have artificially elevated the

concentrations of nutrients in the treatments that

contained jellyfish, relative to the controls. Given that

both species of jellyfish prey on zooplankton, albeit in

different relative abundances (Pitt, unpublished data),

the retention of the zooplankton probably had minimal

influence on comparisons between species. Overall

the biomass of zooplankton on the oral arms of the

animals would have been small and we consider that it

would have had minimal influence on the results.

5. Ecological implications

Gelatinous zooplankton are voracious predators

and their intense predation on zooplankton can

indirectly enhance abundances of phytoplankton

because it reduces the grazing pressure of herbivo-

rous zooplankton on phytoplankton—so-called btop-downQ control (e.g., Olsson et al., 1992). Excretion

of inorganic nutrients by gelatinous zooplankters

may, however, simultaneously promote growth of

phytoplankton in areas where nutrients are limiting

(Biggs, 1977). Gelatinous zooplankters may, there-

fore, influence phytoplankton dynamics by a combi-

nation of btop-downQ and bbottom-upQ controls (e.g.,Deason and Smayda, 1982). C. mosaicus and P.

punctata capture similar zooplankton taxa on their

oral arms (Pitt, unpublished data) and so, like most

medusae, both of these species probably also exert

top-down control on zooplankton and phytoplankton

populations. Excretion of nitrogenous wastes by C.

mosaicus may also promote growth of phytoplank-

ton in regions where nitrogen is limiting, simulta-

neously enabling bottom-up control. In contrast, P.

punctata excreted little NH3 and PO4 and, although

it excreted more NOx than C. mosaicus, the actual

quantities excreted were small. Hence, unlike C.

mosaicus, P. punctata probably exerts minimal

bottom-up influence.

Nutrient cycling in estuaries is a dynamic process

that varies temporally and spatially. Variability arises

from, among other things, meteorological forcing

(Chapelle et al., 2000) and the nature of the sediments

and type of plants present (Eyre and Ferguson, 2002).

Such spatio-temporal variability makes it difficult to

quantify the relative contributions of different com-

ponents to nutrient recycling. Efflux from sediments is

generally considered a major source of recycled

inorganic nitrogen, but if nitrogen is recycled to the

water column in gaseous form through denitrification

(i.e., as N2), it is largely lost from the system and is

bio-available only to nitrogen-fixing organisms such

K.A. Pitt et al. / J. Exp. Mar. Biol. Ecol. 315 (2005) 71–8684

as cyanobacteria (Eyre and Ferguson, 2002). The

nitrogen excreted by jellyfish (predominantly NH3–N)

is in a form that is readily utilised by primary

producers and, therefore, when jellyfish are abundant,

they are likely to be an important source of bio-

available forms of nitrogen for primary producers.

The influence of medusae on nutrient recycling will

be proportional to the size of their populations. Large

and rapid fluctuations in abundances are characteristic

of jellyfish populations. For example, in 1998 in Lake

Illawarra, a coastal lagoon 80 km south of Sydney that

has a surface area of 35 km2, there was a 30-fold

increase in the abundance of C. mosaicus over a period

of just 6 weeks (Pitt and Kingsford, 2000), with the

biomass of the population bloom conservatively

estimated at 18,000 tonnes (Pitt and Kingsford,

2003). If we assume that rates of excretion of NH3

measured in Smiths Lake were similar to those of

medusae in Lake Illawarra at the time of the bloom,

then our measurements of inorganic nutrient cycling

by C. mosaicus allow us to estimate the importance of

these organisms for nutrient regeneration in Lake

Illawarra. The measured ammonia regeneration rates

of 1505 Ag NH3 kg�1 h�1 (light) and 1016 Ag NH3

kg�1 h�1 (dark) give a daily nutrient regeneration rate

of 30 mg NH3 kg�1 day�1 assuming equal day/night

length of 12 h. At times of peak jellyfish biomass

measured as around 18,000 tonnes, this gives an

excretion rate of 540 kg day�1 for the estuary as a

whole or a rate of 15 mg NH3 m�2 day�1, equivalent to

13 mg NH3–N m�2 day�1. Detailed studies by S.

Wellman (University of Newcastle, Australia; personal

communication) of primary production in the estuary

suggest that a typical primary production rate for the

estuary is about 1000 mg C m�2 day�1. Using the

Redfield ratio of 6.6 for C/N of phytoplankton, this

suggests that phytoplankton produces 152 mg N m�2

day�1. Comparison with the measured ammonia–N

excretion rate of C. mosaicus shows that NH3–N

excretion can account for about 8% of the inorganic

nitrogen requirements of phytoplankton consumers in

this system.

Further studies by the NSWDepartment of Environ-

ment and Conservation (Potts, personal communica-

tion) have shown that sediment regeneration of NH3–N

averages 4 mmol NH3–N m�2 day�1 during the day

and 13 mmol NH3–N m�2 day�1 at night giving an

average daily flux rate of 9 mmol NH3–N m�2 day�1.

Again, comparing these measured rates with the

ammonia regeneration rates of C. mosaicus shows that

ammonia regeneration by the jellyfish amounts to

about 11% of the measured ammonia regeneration

rates from sediments, generally believed to be the

primary source of inorganic nutrients to this system.

The figures calculated above are likely to be

conservative because the average size of medusae

during the population bloom upon which the figures

were calculated was very small (77 mm BD; Pitt and

Kingsford, 2003). Given that rates of excretion are

usually negatively correlated to size (Matsakis, 1992)

and that excretion rates were determined for much

larger animals (mean 209 mm BD), excretion by the

medusae during the bloom was probably greater than

estimated for the large adult medusae used in the

current study. Measurements of how rates of excretion

vary with size are required.

The degree of flushing of an estuary will also affect

the relative contribution of excretion by jellyfish to

nutrient recycling. Diverse types of estuaries occur

along the east coast of Australia, ranging from marine-

dominated, open embayments that are well flushed, to

shallow coastal lagoons that have minimal riverine

input and only open to the sea after periods of heavy

rain cause the entrances of the lagoons to breach (Roy

et al., 2002). C. mosaicus and P. punctata occur in

many different types of estuaries, but their influence

on nutrient recycling will vary, depending on the

degree of flushing of the estuary. Excretion of

nitrogenous compounds by C. mosaicus, in particular,

will have a far greater effect in lagoons that are

isolated from the sea and poorly flushed.

There is growing evidence that populations of

gelatinous zooplankton are increasing globally (Mills,

2001), either due to the introduction of exotic species

into new regions (Shiganova, 1998) or due to

increases in the biomass of populations in their native

environments (Brodeur et al., 2002). In Australia,

populations of C. mosaicus and P. punctata some-

times form blooms (Pitt and Kingsford, 2003),

although due to the lack of long-term data, it is not

possible to determine whether this represents a generic

increase in biomass. If, indeed, populations of

medusae are increasing, then, in addition to their

intense grazing, azooxanthellate species, or those with

relatively few symbionts, are also likely to have a

major influence on nutrient recycling.

K.A. Pitt et al. / J. Exp. Mar. Biol. Ecol. 315 (2005) 71–86 85

Acknowledgments

We are very grateful to J. Grayson, J. Browne, B.

Clynick and P. Barnes for their tireless efforts in the

field. Thanks also to G. Coade for preparing nutrients

and useful discussion, S. Wellman for analysing the

nutrient samples, A. Redden for use of her filtering

equipment and T. Glasby for helpful discussion

regarding experimental design. We also wish to thank

The University of Sydney for use of their facilities.

The project was conducted at the University of New

South Wales’ Smiths Lake Field Station and was

funded by an Australian Research Council Strategic

Partnership-Industry Training and Research grant

awarded to M. Kingsford, K. Pitt, K. Koop and D.

Rissik. [SS]

References

Balderston, W.L., Claus, G., 1969. A study of the symbiotic

relationship between Symbiodinium microadriaticum Freuden-

thal, a zooxanthella, and the upside down jellyfish Cassiopea

spec. Nova Hedwig. 17, 373–382.

Biggs, D., 1977. Respiration and ammonium excretion by open

ocean gelatinous zooplankton. Limnol. Oceanogr. 22, 108–117.

Brodeur, R., Sugisaki, H., Hunt, G.J., 2002. Increases in jellyfish

biomass in the Bering Sea: implications for the ecosystem. Mar.

Ecol., Prog. Ser. 233, 89–103.

Cates, N., McLaughlin, J.A.J., 1976. Differences of ammonia

metabolism in symbiotic and aposymbiotic Condylactus and

Cassiopea spp. J. Exp. Mar. Biol. Ecol. 21, 1–5.

Chapelle, A., Menesguen, A., Deslous-Paoli, J.-M., Souchu, P.,

Mazouni, N., Vaquer, A., Millet, B., 2000. Modelling nitrogen,

primary production and oxygen in a Mediterranean lagoon.

Impact of oyster farming and inputs from the watershed. Ecol.

Model. 127, 161–181.

Deason, E., Smayda, T., 1982. Ctenophore–zooplankton–phyto-

plankton interactions in Narragansett Bay, Rhode Island, USA,

during 1972–1977. J. Plankton Res. 4, 203–217.

Eyre, B.D., Ferguson, A.J.P., 2002. Comparison of carbon

production and decomosition, benthic nutrient fluxes and

denitrification in seagrass, phytoplankton, benthic microalgae-

and macroalgae-dominated warm–temperate Australian lagoons.

Mar. Ecol., Prog. Ser. 229, 43–59.

Ikeda, T., 1985. Metabolic rates of epipelagic marine zooplankton as

a function of body mass and temperature. Mar. Biol. 85, 1–11.

Ikeda, T., Mitchell, A.W., 1982. Oxygen uptake, ammonia excretion

and phosphate excretion by krill and other Antarctic zooplank-

ton in relation to their body size and chemical composition. Mar.

Biol. 71, 283–298.

Kremer, P., 1977. Respiration and excretion by the ctenophore

Mnemiopsis leidyi. Mar. Biol. 44, 43–50.

Kremer, P., 1982. Effect of food availability on the metabolism of

the ctenophore Mnemiopsis mccradyi. Mar. Biol. 71, 149–156.

Matsakis, S., 1992. Ammonia excretion rate of Clytia spp.

hydromedusae (Cnidaria Thecata): effects of individual dry

weight, temperature and food availability. Mar. Ecol., Prog. Ser.

84, 55–63.

Matsakis, S., Conover, R.J., 1991. Abundance and feeding of

medusae and their potential impact as predators on other

zooplankton in Bedford Basin (Nova Scotia, Canada) during

spring. Can. J. Fish. Aquat. Sci. 48, 1419–1430.

McCloskey, L.R., Muscatine, L., Wilkerson, F.P., 1994. Daily

photosynthesis, respiration, and carbon budgets in a tropical

marine jellyfish (Mastigias sp.). Mar. Biol. 119, 13–22.

Miller, D., Yellowlees, D., 1989. Inorganic nitrogen uptake by

symbiotic marine cnidarians: a critical review. Proc. R. Soc.

London, Ser. B 237, 109–125.

Mills, C.E., 2001. Jellyfish blooms: are populations increasing

globally in response to changing ocean conditions? Hydro-

biologia 451, 55–68.

Muscatine, L., Marian, R.E., 1982. Dissolved inorganic nitrogen

flux in symbiotic and nonsymbiotic medusae. Limnol. Oceanogr.

27, 910–917.

Olsson, P., Graneli, E., Carlsson, P., Abreu, P., 1992. Structuring of

a postspring phytoplankton community by manipulation of

trophic interactions. J. Exp. Mar. Biol. Ecol. 158, 249–266.

Pages, F., White, M.G., Rodhouse, P.G., 1996. Abundance of

gelatinous carnivores in the nekton community of the Antarctic

Polar Frontal Zone in summer 1994. Mar. Ecol., Prog. Ser. 141,

139–147.

Pages, F., Gonzalez, H.E., Ramon, M., Sobarzo, M., Gili, J.-M.,

2001. Gelatinous zooplankton assemblages associated with

water masses in the Humboldt Current System, and potential

predatory impact by Bassia bassensis (Siphonophora: Calyco-

phorae). Mar. Ecol., Prog. Ser. 210, 13–24.

Pitt, K.A., Kingsford, M.J., 2000. Geographic separation of stocks of

the edible jellyfish Catostylus mosaicus (Rhizostomeae) in New

South Wales, Australia. Mar. Ecol., Prog. Ser. 136, 143–155.

Pitt, K.A., Kingsford, M.J., 2003. Temporal variation in the virgin

biomass of the edible jellyfish, Catostylus mosaicus (Scypho-

zoa, Rhizostomeae). Fish. Res. 63, 303–313.

Priddle, J., Whitehouse, M.J., Ward, P., Shreeve, R.S., Brierley,

A.S., Atkinson, A., Watkins, J.L., Brandon, M.A., Cripps, G.C.,

2003. Biogeochemistry of a Southern Ocean plankton ecosys-

tem: using natural variability in community composition to

study the role of metazooplankton in carbon and nitrogen

cycles. J. Geophys. Res. 108 (C4), 8082.

Reissig, M., Queimalinos, P., Balseiro, E.G., 2003. Effects of

Galaxias maculatus on nutrient dynamics and phytoplankton

biomass in a North Patagonian oligotrophic lake. Environ. Biol.

Fish. 68, 15–24.

Roy, P.S., Williams, R.J., Jones, A.R., Yassini, I., Gibbs, P.J.,

Coates, B., West, R.J., Scanes, P.R., Hudson, J.P., Nichol, S.,

2002. Structure and function of south-east Australian estuaries.

Estuar. Coast. Shelf Sci. 53, 351–384.

Schneider, G., 1989. The common jellyfish Aurelia aurita: standing

stock, excretion and nutrient regeneration in the Kiel Bight,

Western Baltic. Mar. Biol. 100, 507–514.

K.A. Pitt et al. / J. Exp. Mar. Biol. Ecol. 315 (2005) 71–8686

Shiganova, T.A., 1998. Invasion of the Black Sea by the ctenophore

Mnemiopsis leidyi and recent changes in pelagic community

structure. Fish. Oceanogr. 7, 305–310.

Underwood, A.J., 1997. Experiments in Ecology: Their Logical

Design and Interpretation Using Analysis of Variance. Cam-

bridge University Press, Cambridge.

Uthicke, S., 2001. Nutrient regeneration by abundant coral reef

holothurians. J. Exp. Mar. Biol. Ecol. 265, 153–170.

Verde, E.A., McCloskey, L.R., 1998. Production, respiration, and

photophysiology of the mangrove jellyfish Cassiopea xama-

chana symbiotic with zooxanthellae: effect of jellyfish size and

season. Mar. Ecol., Prog. Ser. 168, 147–162.

Wilkerson, F.P., Kremer, P., 1992. DIN, DON and PO4 flux by a

medusa with algal symbionts. Mar. Ecol., Prog. Ser. 90,

237–250.