Superfluous Feeding and Growth of Jellyfish Aurelia aurita

Abstract

According to a recently presented bioenergetic model for the weight-specific growth rate of jellyfish, Aurelia aurita, fed brine shrimp, Artemia salina, the specific growth will remain high and constant at prey concentrations > 6 Artemia l⁻¹. The aim of the present study was to verify this statement by conducting controlled feeding and growth experiments on small jellyfish in tanks. It was found that prey organisms offered in concentrations of 25, 50, and 100 Artemia l⁻¹ resulted in specific growth rates in fair agreement with the model-predicted rates. The high prey concentrations resulted in superfluous feeding and production of pseudofeces which indicated that not all captured prey organisms were ingested but instead entangled in mucus and dropped. The high prey concentrations did not influence the filtration rate of the jellyfish.

1. Introduction

The common filter-feeding jellyfish Aurelia aurita occurs in many coastal ecosystems and can be very abundant and exert a considerable predatory impact on zooplankton [1,2,3,4,5,6,7,8,9]. A. aurita swims by means of umbrella pulsation and prey organisms are captured by tentacles on the bell rim during the recovery stroke [10]. A. aurita has a life cycle that includes a pelagic medusa and a benthic polyp stage. Medusae reproduce sexually, and females release planula larvae that settle and metamorphose into polyps that produce ephyrae that develop into medusae [11,12]. In temperate waters, an annual life cycle of A. aurita is typical [12,13]. Thus, in temperate Danish waters, ephyrae are released in spring resulting in a distinct cohort of medusae that reproduce sexually during summer, followed by loss of body mass (“degrowth”) and disappearance of medusae in late autumn [14,15].

The population density and individual size of Aurelia aurita have over the years been investigated in the shallow semi-enclosed Danish cove Kertinge Nor [14,15,16]. In this cove, the numerous medusae are characterized by their small umbrella diameter. The population predation impact exerted by numerous small A. aurita, with estimated zooplankton half-lives of only about 1 to 3 d, indicates that shortage of prey controls the maximum umbrella size of typically 30 to 50 mm in Kertinge Nor [14,15], although in some years up to 60 to 70 mm [16] before subsequent degrowth.

In a recent study, [17] presented a bioenergetic model for the weight-specific growth rate of Aurelia aurita fed on 3-day-old brine shrimp Artemia salina as a reference prey organism. According to this model, the specific growth rate increases linearly with prey concentration in the range of 1 to 6 Artemia l⁻¹ but remains high and constant at prey concentrations > 6 Artemia l⁻¹. The aim of the present study was to verify this last-mentioned statement by conducting controlled feeding and growth experiments in tanks with small food-limited jellyfish from Kertinge Nor exposed to various high prey concentrations resulting in superfluous feeding.

2. Materials and Methods

2.1. Collection of Jellyfish

Small (<65 mm umbrella diameter) jellyfish, Aurelia aurita, were collected on 3 June 2022 in Kerting Nor, Denmark, and brought to the nearby Marine Biological Research Centre for feeding and growth experiments.

2.2. Laboratory Feeding and Growth Experiments

Jellyfish were kept in tanks and continuously fed with 3-day-old Artemia salina nauplii obtained from cysts. Therefore, every day a new cohort of A. salina was started in air-mixed 3 l flasks. A. salina nauplii were transferred to a magnetic stirrer mixed 10 l stock culture in glass flask. By means of a peristaltic pump, the Artemia prey organisms were continuously dosed from the stock flask to the jellyfish growth tank and the same water volume (6.5 ml min⁻¹) was simultaneously taken out by another channel of the dosing pump. All experiments were conducted at 13 °C in a temperature-controlled aquarium hall and 20 psu as measured at the collecting site.

The wanted steady-state prey concentrations of 25, 50, and 100 Artemia l⁻¹ in 3 parallel growth experiments (Exp #1, #2 and #3) were ensured by adjusting the number of Artemia added to the 12 l jellyfish tank to match the steadily increasing clearance rate of the growing jellyfish during the experimental period. Every day all jellyfish were carefully taken out and placed with the aboral side on a millimeter paper to measure their umbrella diameter. The concentration of prey organisms in each of the jellyfish growth tanks was measured every day by taking out samples for counting under a stereo microscope to adjust the number of prey organisms that had to be added to maintain the wanted mean concentration. The experiments were started on 7 June 2022 with 6 small jellyfish in each of the 3 tanks (50 cm diameter Breeding Air Kreisel, Schuran Seawater Equipment, www.schuran.com, accessed on 18 September 2022) with slowly air-driven circulating seawater to keep the jellyfish freely and undisturbed swimming. The feeding experiments ran for 17 d.

2.3. Equations

In a recent study, Ref. [17] set up the following bioenergetic model for weight-specific growth rate of Aurelia aurita fed on 3-day-old Artemia salina: µ = (n × 0.07 − 0.08)W^−0.2, where W (mg) is the jellyfish dry weight and n is the number of Artemia l⁻¹ in the range of 1 to 6 Artemia l⁻¹. At prey concentrations > 6 Artemia l⁻¹ the model conforms to:

µ_model = (6 × 0.07 − 0.08)W^−0.2 = 0.34W^−0.2.

(1)

The aim of the present study was to verify if this simple growth model applies to superfluous feeding jellyfish.

The filtration rate (=clearance rate, F_exp) of jellyfish in the tanks was experimentally measured by the steady-state method which is based on the principle: [prey organisms removed by jellyfish (F_est × C_c)] = [number of prey organisms dosed from stock-culture flask (Fl × C_p) − prey washed out with outflowing seawater (Fl × C_c)], so that:

F_exp = (Fl × C_p − Fl × C_c)/C_c,

(2)

where Fl = dosing pump rate, C_p = concentration of Artemia in stock-culture flask, C_c = concentration of Artemia in jellyfish tank.

The average size of Aurelia aurita during the growth period was estimated as:

W_avg = (W₀ × W_t)^1/2,

(3)

where W₀ and W_t express the mean individual body dry weight of jellyfish at time t₀ and time t_t, respectively.

The following allometric equation was used to estimate dry weight (W, mg) from umbrella diameter (d, mm) of Aurelia aurita medusae (≥10 mm), [14]:

W = 1.73 × 10⁻³ × d^2.82.

(4)

The following equation for filtration rate (F_model, l d⁻¹) of Aurelia aurita fed on 3-day Artemia as a function of dry weight W (mg) was used in the bioenergetic model [17] and adapted from [7]:

F_model = 3.9W^0.78.

(5)

3. Results

The increase in the size of Aurelia aurita fed 25, 50, and 100 Artemia l⁻¹ are shown in Figure 1, Figure 2 and Figure 3 along with inserted exponential regression lines and their equations. The exponents of the regression equations that express the mean weight-specific growth rates (µ_exp) are shown in Table 1 along with the model-predicted growth rate (µ_model).

Table 1. Aurelia aurita. Experimental data and calculated parameters for feeding and growth experiments (Exp #1, #2, #3). C_c = mean ± s.d. concentration of Artemia prey organisms in the tank. Umbrella diameter on Day 0 = d₀, and on Day 17 = d₁₇. Estimated dry weight on Day 0 = W₀ and on Day 17 = W₁₇ using Equation (4). W_avg = average size during the 17-day time interval estimated as W_avg = (W₀ × W₁₇)^1/2, cf. Equation (3). The predicted mean weight-specific growth rate (µ_model) was estimated using Equation (1). The experimentally determined specific growth (µ_exp) was determined as the b-exponent in the exponential regression equation for lines shown in Figure 1, Figure 2 and Figure 3. Values for µ_exp leaving out the first 3 days are shown in brackets. F_exp = experimentally measured individual filtration rate using Equation (2). F_model = filtration rate estimated using Equation (5).

Exp	Cc (ind. l−1)	d0 (mm)	d17 (mm)	W0 (mg)	W17 (mg)	Wavg (mg)	µmodel (% d−1)	µexp (% d−1)	Fexp (l d−1)	Fmodel (l d−1)
#1	25 ± 10	48 ± 4	82 ± 8	95 ± 21	444 ± 137	170	12.1	10.1 (10.3)	343 ± 130	214
#2	49 ± 11	65 ± 4	101 ± 3	226 ± 41	778 ± 68	419	10.2	8.9 (10.6)	306 ± 100	433
#3	105 ± 70	61 ± 5	86 ± 11	191 ± 39	507 ± 191	331	10.7	5.4 (5.8)	362 ± 153	360

Table 1. Aurelia aurita. Experimental data and calculated parameters for feeding and growth experiments (Exp #1, #2, #3). C_c = mean ± s.d. concentration of Artemia prey organisms in the tank. Umbrella diameter on Day 0 = d₀, and on Day 17 = d₁₇. Estimated dry weight on Day 0 = W₀ and on Day 17 = W₁₇ using Equation (4). W_avg = average size during the 17-day time interval estimated as W_avg = (W₀ × W₁₇)^1/2, cf. Equation (3). The predicted mean weight-specific growth rate (µ_model) was estimated using Equation (1). The experimentally determined specific growth (µ_exp) was determined as the b-exponent in the exponential regression equation for lines shown in Figure 1, Figure 2 and Figure 3. Values for µ_exp leaving out the first 3 days are shown in brackets. F_exp = experimentally measured individual filtration rate using Equation (2). F_model = filtration rate estimated using Equation (5).

Exp	Cc (ind. l−1)	d0 (mm)	d17 (mm)	W0 (mg)	W17 (mg)	Wavg (mg)	µmodel (% d−1)	µexp (% d−1)	Fexp (l d−1)	Fmodel (l d−1)
#1	25 ± 10	48 ± 4	82 ± 8	95 ± 21	444 ± 137	170	12.1	10.1 (10.3)	343 ± 130	214
#2	49 ± 11	65 ± 4	101 ± 3	226 ± 41	778 ± 68	419	10.2	8.9 (10.6)	306 ± 100	433
#3	105 ± 70	61 ± 5	86 ± 11	191 ± 39	507 ± 191	331	10.7	5.4 (5.8)	362 ± 153	360

Because relatively low specific growth rates may be expected in the beginning of the feeding period due to mobilization of digestion processes in the previously starving jellyfish, and further, because possible initial growth in body thickness may take place before subsequent increase in umbrella diameter takes place, the weight-specific growth rates (µ_exp) have also been calculated leaving out the first 3 days and shown in brackets in Table 1. It is seen that these values are somewhat higher and in fair agreement with the model-predicted values (µ_model). Thus, it may be concluded that the simple bioenergetic model Equation (1) applies for small superfluous feeding Aurelia aurita.

The experimentally measured average filtration rates (=clearance rate of 3-day-old Artemia, F_exp) are in fair agreement with the estimated (F_model) using Equation (5) although pseudofeces (mucus entangled with prey organisms) accumulated at the bottom of the tanks (Figure 4). Superfluous feeding took place in all experiments and the amount of pseudofeces accumulated increased with increasing prey concentration, most pronounced in Exp #3. Therefore, the tanks had to be cleaned every 3 to 4 days.

4. Discussion

The growth potential of jellyfish in nature is generally not utilized due to a shortage of food. Thus, the increase in umbrella diameter of Aurelia aurita in the field was compared with “well-fed” jellyfish kept in tanks by [18]. The two groups showed near identical initial values at the start of May but began to diverge in June to become about 80 mm in the field and about 130 mm in the well-fed experiment. A re-plot of the well-fed A. aurita based on the estimated dry weight from umbrella diameter showed a systematic deviation between the data and regression curve because the weight-specific growth rate was not constant but decreased with a size that could be described by a power-function curve with b = −0.24 [17], which is close to the model-predicted b-value of −0.2 in Equation (1).

The present work shows that prey organisms offered in concentrations 4, 8, and 17 times above the lowest of six Artemia l⁻¹, which give rise to maximum growth of Aurelia aurita [17], results in superfluous feeding where a substantial number of the captured prey organisms are not being ingested but become entangled in mucus and dropped as pseudofeces. When the digestive system is filled up with prey the pseudofeces production ensures that the jellyfish may still utilize its growth potential while likewise, the filtration rate remains undisturbed up to at least 100 Artemia l⁻¹ (Table 1). However, it should be stressed that Artemia used here as a reference prey organism is not among the natural zooplankton in the sea, but it is easily available food for cultured predatory organisms such as jellyfish. The 3-day-old Artemia have no escape behavior and are captured by jellyfish with higher efficiency than other prey. Thus, relative to Artemia, retention efficiency has been found to be 60% for rotifers, 35% for adult copepods, 22% for copepod nauplii, and 14% for mussel veligers [19].

The present study emphasizes that jellyfish are continuously filtering the ambient water at high rates and therefore in controlled feeding and growth experiments need to be fed continuously at relatively low prey concentrations. Thus, a mean individual filtration rate of 340 l d⁻¹ or 236 mL min⁻¹ as measured here in a 12 L tank with six jellyfish implies that the half-life of Artemia is: t_1/2 = 12,000/(236 × 6) × ln2 = 5.9 min. If all the prey organisms were offered one daily meal the prey organisms would have a mean residence time of only 5.9 min and would therefore rapidly be captured and most of them subsequently dropped to the bottom as pseudofeces resulting in suboptimal growth. As [14] noticed, when the guts of medusae were filled up with prey organisms at high prey concentrations, that part of the captured prey was killed and “apparently rejected instead of being digested”. Obviously, a better understanding of the rejection and protection processes involved in superfluous feeding is needed, not least because knowledge of the actual prey ingestion rate and assimilation efficiency is important in bioenergetic studies on jellyfish.

5. Conclusions

When Aurelia aurita is offered prey concentrations 4, 8, and 17 times above the lowest needed for maximal growth this gives rise to superfluous feeding by which a substantial number of the captured prey organisms are not being ingested but become entangled in mucus and dropped as pseudofeces. Nevertheless, this does not influence the filtration rate of the jellyfish, which remains high and constant. Likewise, the weight-specific growth rate of A. aurita remains in fair agreement with the model-predicted growth. However, a better understanding of the processes involved in superfluous feeding in jellyfish is needed because knowledge of the actual prey ingestion rate is important in bioenergetic studies.