Clearance rates of ephyrae and small medusae of the common jellyfish Aurelia aurita offered different types of prey

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<ul><li><p>us</p><p>00</p><p>EphyraeMedusaeClearance RateIngestion RateRetention EfciencyAurelia aurita</p><p>ge otimrrengestion-rate method) to estimate the amount of water cleared per unit of time</p><p>1</p><p>Aureli</p><p>Journal of Sea Research 65 (2011) 5157</p><p>Contents lists available at ScienceDirect</p><p>Journal of Se</p><p>e lset al., 1990). High densities of this pelagic gelatinous predator canseriously affect populations of zooplankton and ichthyoplankton andmay be detrimental to sheries through competition for food withshes as well as direct predation on eggs and larvae of sh (Mller,1980; Purcell, 1997; Hansson et al., 2005; Purcell and Decker, 2005).</p><p>Aurelia aurita has a life cyclewith twomorphs, a pelagicmedusa anda benthic polyp (Hernroth and Grndahl, 1985; Papathanassiou et al.,1987; Schneider and Behrends, 1994; Miyake et al., 1997; Ishii andTakagi, 2003). The medusa has sexual reproduction and larval</p><p>the shallowcove of KertingeNor (Denmark). Therst ephyrae appearedinMarch anddisappeared again inMay, and clearly, therewas producedone well-dened year group of A. aurita with a maximum of about400 ind.m3 in May 2009, followed by a general decrease in densityduring the period May to August, probably due to ush out of the coveby water exchange. Natural populations of A. aurita are usually foodlimited (Schneider and Behrends, 1994) and in Kertinge Nor themaximum diameter of the umbrella is usually only a few centimetre(compared to about 30 cm inmost otherwaters) owing to an extremelydevelopment, followed by disappearance ofwater columnand planulametamorphoses intThe time and length of occurrence of the ephlocalities (Miyake et al., 1997). The occurrenc</p><p> Corresponding author. Tel./fax: +45 6532 1433.E-mail address: hur@biology.sdu.dk (H.U. Riisgrd).</p><p>1385-1101/$ see front matter 2010 Elsevier B.V. Aldoi:10.1016/j.seares.2010.07.002a aurita is particularlyoastal waters where it iskton communities (Hay</p><p>1999). In the western Baltic Sea the great majority of ephyrae areproduced in April andMay (Mller, 1980). The development of A. auritaephyrae to medusae was recently followed by Riisgrd et al. (2010) inabundant during summer in North Atlantic crecognized as an important predator in plan1. Introduction</p><p>The cosmopolitan scyphomedusa3.81.4 l h by the clearance method and 3.21.1 l h by the ingestion-rate method. Both methodsshowed that copepods (nauplii and adults) and mussel veligers are captured with considerably lowerefciency, 22 to 37% and 14 to 30%, respectively, than Artemia salina nauplii. By contrast, the waterprocessing rates of ephyrae measured by the clearance method with A. salina nauplii as prey were 3 to5 times lower than those measured by the ingestion-rate method. This indicates that the prerequisite of fullmixing for using the clearance method may not have been fullled in the ephyrae experiments. The studydemonstrates that the predation impact of the young stages of A. aurita is strongly dependent on itsdevelopmental stage (ephyra versus medusa), and the types and sizes of prey organisms. The estimatedprey-digestion time of 1.3 h in a steady-state feeding experiment with constant prey concentration supportsthe reliability of the ingestion-rate method, which eliminates the negative container effects of theclearance method, and it seems to be useful in future jellysh studies, especially on small species/youngerstages in which both type and number of prey can be easily and precisely assessed.</p><p> 2010 Elsevier B.V. All rights reserved.</p><p>areas may be seasonally restricted, mainly occurring either in spring orboth in spring and autumn, or it may be continuous (Bmstedt et al.,adult medusae from theo the polyp benthic stage.yra stage varies betweene of ephyrae in northern</p><p>high abundancerestricting their oet al. 1995; Niels</p><p>The ephyra istentacles (Sullivaseldom studied, acapture efciencet al., 1994; Hans</p><p>l rights reserved.a sp. nauplii as prey by both methods, agreed well, namely1Keywords:of different types and sizes of prey organisms offered to A. aurita ephyrae and small medusae. The meanclearance rates of medusae, estimated with ArtemiAccepted 9 July 2010Available online 18 July 2010</p><p>(clearance method and iClearance rates of ephyrae and small medoffered different types of prey</p><p>Hans Ulrik Riisgrd , Caroline V. MadsenMarine Biological Research Centre (University of Southern Denmark), Hindsholmvej 11, 53</p><p>a b s t r a c ta r t i c l e i n f o</p><p>Article history:Received 9 April 2010Received in revised form 6 July 2010</p><p>Prey selection and knowledAurelia aurita may at certainecosystems with mass occu</p><p>j ourna l homepage: www.ae of the common jellysh Aurelia aurita</p><p>Kerteminde, Denmark</p><p>f the amounts of water processed by the early stages of the common jellyshes of the year be crucial for understanding the plankton dynamics in marinences of this jellysh. In the present study we used two different methods</p><p>a Research</p><p>ev ie r.com/ locate /searesof small medusae causing shortage of prey and thuswn growth (Olesen et al., 1994; Olesen, 1995; Riisgrden et al., 1997).typically smaller than 10 mm in diameter and lacksn et al., 1997).The ephyra stage in A. aurita's life cycle isnd information on their abundance, feeding rate, prey-y, and population predation impact is limited (Olesenson et al., 2005; Mller and Riisgrd, 2007b,c).</p></li><li><p>52 H.U. Riisgrd, C.V. Madsen / Journal of Sea Research 65 (2011) 5157Feeding of jellysh predators is characterized by selectivity, whichdepends onmany factors such asprey size and swimming speed, predatortentacle length, width and spacing, predator swimming behavior andresulting bell-margin water ow, nematocyst types affecting penetrationof prey with different vulnerability to toxin and escape abilities (Costelloand Colin, 1994; Ford et al., 1997; Purcell, 1997; Sullivan et al., 1997;Suchman, 2000). The A. aurita ephyrae capture a variety of prey types(Stoecker et al., 1987; Mller 1989; Bmstedt, 1990; Olesen et al., 1994;Olesen, 1995; Sullivan et al., 1994, 1997; Hansson, 2006), but prey size,prey-escape speed, and surface properties of prey strongly inuence thecapture efciency. Thus, using video observations of free-swimmingephyrae and their prey, Sullivan et al. (1997) observed that captureefciencies of ephyrae feeding on large prey (barnacle nauplii, brineshrimp, hydromedusae) were 4 to 12 times greater than for small preytypes (rotifers, copepod nauplii), and further, that capture efciencies forprey of equal sizes differed, indicating that factors in addition to sizeinuence the predatorprey interaction. Likewise, Mller and Riisgrd(2007c) found that the measured clearance rates of A. aurita wereconsiderably higher on 3-day old Artemia nauplii than on 1-day oldArtemia.</p><p>In ecological studies, prey-selection mechanisms are important forunderstanding how jellysh predationmay alter the zooplankton speciescomposition (Costello and Colin, 1994; Purcell, 1997; Ford et al., 1997),and likewise, knowledge of the actual amounts of prey eaten by thejellysh is crucial to understand the plankton dynamics in marineecosystems with frequent mass occurrences of jellysh (Olesen et al.,1994; Hansson et al., 2005;Mller and Riisgrd, 2007a,b,c; Purcell, 2009).</p><p>In the present study, we used two fundamentally differentmethods, the clearance method and the ingestion-rate method,to determine the amount of water cleared per unit of time of differenttypes of prey organisms offered to A. aurita ephyrae and smallmedusae. This approach enabled us to evaluate the relative prey-capture efciency of the early jellysh stages, and to evaluate themerits of the two clearance methods.</p><p>2. Materials and methods</p><p>2.1. Prey organisms</p><p>The jellysh used in the clearance experiments were offereddifferent types of cultivated prey organisms: brine shrimp nauplii(Artemia salina), nauplii and adult copepods (Acartia tonsa), rotifers(Brachionus plicatilis), and mussel veligers (Mytilus edulis). All preyorganisms were fed a monoculture of Rhodomonas sp. Freshly-collected barnacle cypris larvae (Semibalanus balanoides) were offeredas prey in some clearance experiments.</p><p>2.2. Clearance method</p><p>Ephyrae and small medusae of A. auritawere collected in Februaryand July of 2005, respectively, from Kertinge Nor, a shallow cove onthe east coast of the island of Fyn, Denmark. The jellysh werebrought to the laboratory and kept in storage aquaria (15 C; 20 psu)until experiments could be performed. If kept for longer than a fewdays, the jellysh were fed A. salina nauplii.</p><p>A. aurita (ephyrae andmedusae) clearance rates were measured inlaboratory experiments as the volume of water cleared of preyorganisms per unit time. A known number of prey organisms wereadded to 3 to 7 experimental tanks with known volumes (V) ofltered seawater. By using a pipette, big drops of water with preyfrom the cultivating tankwere placed on the bottom of a Petri disc andthe number of prey organisms in each drop was counted so that theexact number of prey, subsequently added by washing all the dropsinto the experimental tank, was known. At time zero, jellysh (3 to 9ephyrae or 1 medusa) were added to each experimental tank, and one</p><p>tank without jellysh served as control. For ephyrae 0.2 to 0.8 l ofltered seawater was added to a glass beaker; for medusae, 6 l ofwater was added to an aquarium. The reduction in the number of preyorganisms as a function of timewas followed by removing the jellyshfrom one aquarium at time intervals and ltering (80-m mesh) allthe water (i.e. data for each aquarium represents 1 time); the retainedprey organisms were counted by use of a stereo-microscope. Theindividual clearance rate (Cl, ml h1) was determined from theexponential reduction in prey concentration from the formula:</p><p>Cl = aV = n; 1</p><p>where a=slope of the tted regression line in a plot of lnCt versus time,n=number of jellysh in the experimental tank, V (ml)=volume ofseawater in tank, and Ct is prey concentration at time t. All experimentswere conducted at 15 C and 20 psu.</p><p>2.3. Ingestion-rate method</p><p>Ephyrae and small medusae of A. auritawere collected in April andJuneJuly 2009, respectively, from Kertinge Nor. The jellysh werebrought to the laboratory and kept in storage aquaria until experi-ments could be performed. If kept for longer than a few days, thejellysh were fed A. salina nauplii.</p><p>A known number of jellysh were carefully transferred in a beakerwith water to the experimental tank containing a known volume ofseawater (60 or 70 l) and allowed to acclimate to the ambient watersalinity and temperature (20 psu, 12.4 C) for some hours, until theundisturbed jellysh were swimming freely around in the water and novisible zooplankton remained in the gastric pouches of the medusae. Attime zero, 3 types of prey organisms were added in the sameconcentration (C) of 10 prey l1. Every 10 min afterwards, one or severaljellysh were taken out (and not later returned), and the number of eachtype of prey seen in the stomach were counted by use of a stereo-microscope. The ingestion rate (I, prey min1) was determined from theslope of the regression line based on the number of prey in the stomach asa function of time. The clearance rate (Cl, l h1) then was determined as:</p><p>Cl = I 60 = C 2</p><p>A precondition for using the equation is that the prey concentra-tion remains constant throughout the experimental time. This wasapproximated by use of the large tank volume so that the preyconcentration remained approximately constant during the experi-ment; no more than 15% of the prey organisms were removed by theend of the experiment.</p><p>Because it was important to count all the prey ingested, theoptimum concentration for the experimental procedure was initiallydetermined. Jellysh may regurgitate their stomach contents if theprey concentration is too high. Preliminary tests with differentconcentrations of A. salina nauplii showed that regurgitation did notoccur at or below 10 prey l1. To ensure that the number of each preytype in the stomach could be identied, the experimental period was60 min. Prey organisms were classied as digested when no solidmaterial was seen in the stomach.</p><p>2.4. Steady-state experiment and digestion time</p><p>In steady state (i.e. ingestion rate of prey=digestion rate of prey), theingestion rate (I, prey h1), clearance rate (Cl, l ind.1 h1), number ofprey in the gastric pouches of themedusae (G), prey concentration in theambient water (C, prey l1), and prey-digestion time (E, h) areinterconnected and can be expressed by the following equations:</p><p>I = G= E 3</p><p>Cl = I = C 4</p></li><li><p>The number of prey organisms (A. salina nauplii) in the gut of A.aurita (343 mm in diameter) was monitored during a 3-h experi-ment in which 6 medusae were removed every 60 min from a 70-laquarium with 10 prey l1.</p><p>3. Results</p><p>3.1. Clearance method</p><p>Fig. 1 shows two examples of clearance experiments with A. auritaephyrae. Clearance rates of A. aurita ephyrae were measured inexperiments in which different types of prey, i.e. copepods (naupliiand adults), barnacle cypris larvae, and hydromedusae were providedsimultaneously (Fig. 2). The clearance rate measured for ephyraefeeding on adult copepods (0.8 ml h1 ind.1) was very low comparedto the clearance on copepod nauplii (about 14 ml h1 ind.1). Ephyraeretained adult copepods and barnacle cypris larvae at very low rates ascompared with Artemia nauplii (Table 1). Furthermore, the clearancerates of Artemia and rotifers increased with increasing ephyra size. Forephyrae of same size (i.e. 5.1 to 5.2 mm diameter), the estimated meanclearance rates were 54.417.2 ml h1 (n=9) for Artemia, 23.010.0 ml h1 (n=3) for rotifers, and 18.915.0 ml h1 (n=5) forcopepod nauplii. Thus, rotifers and copepod nauplii are cleared with 42and 35% efciency, respectively, in relation to Artemia. Estimatedclearance rates of A. aurita medusae simultaneously provided withdifferent prey organisms showed the relative retention efciencieswereabout 37 and 16% for nauplii and adult copepods, respectively, and 30%for mussel veligers, as compared with Artemia nauplii as the reference(Fig. 3, Table 2).</p><p>(Tables 3, 4). The clearance rates of A. aurita medusae feeding ondifferent prey organisms showed that the relative retention efcien-cies, as compared with Artemia (0.7 mm),were about 60% for rotifers,35 and 22% for copepod adults and nauplii, and 14% for musselveligers (Tables 5, 6).</p><p>3.3. Steady-state experiment and digestion time</p><p>The mean (SD) numbers of prey in the gut were 38.014.9(n=6), 46.56.8 (6), and 44.09.3 (6) after 1, 2, and 3 h,respectively, and the overall mean in the steady-state period wasG=42.84.4 (n=3). The clearance rate (Table 6) was measured tobe Cl=3.2 l h1 so that I=ClC=3.210=32 prey h1, and thus,the prey-digestion time is estimated at E=G/I=42.8/32=1.3 h,which is in good agreement with the actually observed digestion timefor A. salina nauplii.</p><p>4. Discussion</p><p>The clearance rates reported here compare well with the previouslimited data on the youngest stages of A. aurita (Olesen et al., 1994;Olesen, 1995; Hansson et al., 2005; Mller and Riisgrd, 2007a,b,c).We demonstrated that the clearance rates...</p></li></ul>

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