Oxygen Consumption Rates and Metabolic Enzyme Activities of Oceanic California Medusae in Relation to Body Size and Habitat Depth

15 Pages·1994·6.7 MB·English

by  E V Thuesen

Reference: BioL Bull. 187: 84-98. (August, 1994)
Oxygen Consumption Rates and Metabolic Enzyme
Activities of Oceanic California Medusae in Relation
to Body Size and Habitat Depth
ERIK V. THUESEN1 AND JAMES J. CHILDRESS
Oceanic Biology Group, Marine Science Institute, University of California, Santa Barbara,
California 93106
Abstract. Oxygen consumption rates were measured in in contrast to the rapid declines in metabolic rates and
14 speciesofhydromedusaeand 5 speciesofbathypelagic metabolic potentials with depth that have been observed
coronate scyphomedusae. Analysis of all individuals of for pelagic fishes and crustaceans. Deep-living medusae
all species ofmedusae showed the familiar pattern ofde- have metabolic rates ofa magnitude similar to those of
creasing specific oxygen consumption rate with increasing bathypelagic fishes and crustaceans.
wet weight ofanimals. Citrate synthase (CS), lactate de-
hydrogenase (LDH), malate dehydrogenase (MDH), and
pyruvate kinase (PK) activities were measured in more Introduction
than 30 species of medusae. Octopine dehydrogenase,
Previousstudieson the metabolicratesofmedusae have
strombine dehydrogenase, and alanopine dehydrogenase been mainly restricted to the more common near-shore
were not detected in either hydromedusae or scyphome-
deacuntsziavyei.mtyeTihancetliaavlritglieoermse.itnrLdiiDcviHsdcuaaalclitsnivgwitpaihsese,onboosnmeretvnheeodnoitnohefKrdreehcbarsnedac,syicinlnge- cvsieptseetcdiigetashtei(reoe.nigs.n,)o.AnrTadhiee.epf-1el9wi8v6pi;hnygLsaigroelslooagnti,icnao1lu9s8a7nobdr,gbaainnoidcshmersmefiiecnracellnucidenes-
creased with increasing wet weight. Most medusae were measurementsofthe /'/;siturespiration ofthebathypelagic
aerobically poised, with higher CS activities than LDH scyphomedusa Pom/in rufescens (Smith, 1982); the met-
activities. However, several meso- and bathypelagic me- abolic ratesofthe midwaterctenophore Bathocyroefosteri
(Youngbluth et a/., 1988); and the oxygen consumption
dusae, including the coronate scyphozoans Periphylla
periphyllaandNausithoerubra, wereanaerobicallypoised, rateofthegelatinouspelagic holothuroid Scotoanasxasp.
possibly as a mechanism to assist in vertical migrations from the benthic boundary layer offsouthern California
at low oxygen concentrations in the oxygen minimum (Childresseta/.. 1989). In addition, werecently measured
loaxyyegr.enThceornesiusmppotoironcorrraetelsatiinonthbeestewemeenduCsSaeactwihvietniescoamn-d tnhoeusrepsopliyrcathoareyteraPtoeesoahnidusemnezsyemreesaactnidvistioemseofotthheergdeelaetpi--
pared to previously investigated animals. To account for sea worms and chaetognaths (Thuesen and Childress,
tdhuissapnooCrScaotrrtehleatpieorni,phweeryproofptohseemtahexihympuotmhedsiifsfutshiaotnmdies-- 199O3nae. mb)e.thod ofestimating aerobic metabolic rates from
tance may be oxygen-limited and does not function at enzymaticactivities involves measurement oftheactivity
ofthe electron transport system (ETS) (Bamstedt, 1980;
the normal in vivo rate. For pelagic medusae, there is no
atipapl,arasendtetdeerclmiinneedinbmyeetnazbyomliactircataectainvidtym,ewtiatbholiinccrpeoatseinn-g vMPaaarcyikzoaaurusddt,eytpe1asl9.8.o6f;19z8oP8oa)pc.klaaTrnhdki.tsonm1.9e7ti9hn;coldPuadhciaknsagrbtdehreeenteacsiplpp.e.lcii1ee9ds75to;of
depth ofoccurrence, beyond the declines caused by the
epipelagic hydromedusae by King and Packard (1975).
decrease in temperature with depth. These patterns are
They observed lower metabolic potentials (ETS activities)
in relation to oxygen consumption for medusae than for
Received 14September 1993;accepted 6June 1994.
1 Presentaddress:TheEvergreenStateCollege,Olympia.Washington other zooplankton. There are no previous studies on the
98505. metabolic enzvme activities ofmedusae.
84
METABOLIC CHARACTERISTICS OF CALIFORNIA MEDUSAE 85
Many investigators have observed large declines in the another group ofpelagic organisms that do not have im-
metabolic rates ofpelagic fishes and crustaceans with in- age-forming eyes. Gelatinous organisms are important
creasinghabitat depth (Childressand Thuesen, 1992). The components ofpelagicecosystems, and yetthey have his-
oxygen consumption and nitrogen excretion rates ofpe- torically been overlooked orunderestimated in studieson
lagic crustaceans and the metabolic rates and metabolic marine ecosystems. In the last decade, the quantitative
potentials, as estimated by enzyme activities, of pelagic importance ofmedusae, ctenophores, salps, and otherge-
fishes,decline rapidly with increasingdepthofoccurrence latinous animals in the flow of energy through pelagic
(Childress, 1971, 1975; Childress and Somero, 1979; ecosystems has been recognized (Alldredge, 1984; Long-
Cowlesetal.. 1991;Ikeda. 1988; Quetin ct a/., 1980; Sul- hurst, 1985). This study is a broad comparison of the
livan and Somero, 1980; Torres el a/.. 1979; Torres and metabolic rates and potentials ofoceanic hydromedusae
Somero, 1988). Protein contents of pelagic crustaceans and scyphomedusae living at depths down to 2 km. We
andfishesalsodeclineasafunction ofdepthofoccurrence, examinedenzymeactivitiesand metabolic ratesin relation
but to a much lesser extent than metabolic rates and en- to wet weight to determine the influence ofbody size on
zymatic activities (Bailey and Robison. 1986; Childress these parameters; we also looked at the metabolic poise
andNygaard, 1973, 1974;Childressela/.. 1990b; Stickney ofthe medusae in thisstudy bycomparing anaerobic and
and Torres, 1989). Differences in temperature, pressure, aerobic metabolic potentials.
chemical composition, orsize have been estimated to ac-
count foronly asmall fraction ofthedeclines in metabolic Materials and Methods
ratesofthese organisms. The corresponding proportional
Collection ofmedusae
declineofenzymeactivities in fish white muscle indicates
that the decline in metabolic rate is laid down at the sub- Our primary collecting gear was an opening-closing
cellular level (Childress and Somero, 1979; Siebenaller Mother Tucker trawl with a 10-m2 mouth fitted with a
and Yancey, 1984; Somero and Childress, 1980; Sullivan closing30-1 insulated codend(Childresselal., 1978). The
and Somero, 1980; Torres and Somero, 1988). cod end prevented heat shock to animals livingbelowthe
The visual interactions hypothesis has been proposed thermocline and injury due to turbulence while the net
toaccount forthewidely observed metabolicdeclineswith wasbeingbrought tothesurface. Epipelagic medusaewere
habitat depths in pelagic crustaceansand fishes. It suggests occasionally captured by 200-m wire-out oblique tows of
that animals that use visual interactions in predator-prey a 1-m ring net. Collections were carried out on the RV
relationships have high metabolic rates to maintain the Point Sur in the San Clemente Basin during September
robust bodies needed to react rapidlyovertheappreciable 1988 and in an area about 160 km west of Point Con-
distances in which visual interactions take place in high ception, California (123E, 3450' N) in July 1991, and
light environments; whereasanimalsthat live in environ- on cruises ofthe RV New Horizon offPoint Conception
ments where visual interactions are much more limited inJune 1990and FebruaryandJune 1991. Theshipspeed
in distance due to low light levels, or that do not have was kept very low (0.5-1 kn) to decrease turbulence and
image-forming eyes, have experienced reduced selection abrasion in the net and reduce the number of animals
for locomotory capabilities and hence have lower meta- collected inthecodend,therebymaximizingthecondition
bolic rates compared to their visual counterparts (Chil- ofthe gelatinous organisms. Animals were transferred to
5C
dress and Mickel, 1985; Childress el al.. 1980; Childress seawaterupon recovery,quicklyidentifiedtospecies,
ctal.. 1990a). Onetestofthevisual interactionshypothesis and either held for measurements of metabolic rate or
is to examine the metabolic characteristics of nonvisual frozen in liquid nitrogen for later analyses ofenzyme ac-
pelagic animals with regard to increasing habitat depth. tivity in the laboratory. Every effort was made to select
The visual interactions hypothesis suggests that bathy- animalswithempty manubriaandtoremovecommensal
pelagic nonvisual organisms would have metabolic rates or epizoic organisms.
similar to their epipelagic counterparts. We have tested In addition to thesecollections, someanimalswereob-
this hypothesis by examining the metabolic rates and en- tained with thesampling pumps and collectingdevicesof
ROV
zyme activities ofCalifornia chaetognaths in relation to the Monterey Bay Aquarium Research Institute's
depths ofoccurrence, and our observations support the I'entana in Monterey Canyon in August 1990. Neritic,
predictionsofthevisual interactionshypothesis(Thuesen demersal, and epiphytic medusae were occasionally hand-
and Childress, 1993a). Meso- and bathypelagic chaetog- collected in the Santa Barbara Channel by scuba divers
naths have oxygen consumption rates and enzyme activ- over the course ofthis study.
ities comparable to epipelagic species when measured at The demersal hydrozoan Polyorchis penicillatus and
the same temperature. the epipelagic hydrozoan Leukartiam oekmawere main-
Herein we examine the predictions ofthe visual inter- tained in a planktonkreisel with an abundant supply of
actions hypothesis when applied to pelagic medusae crustaceans, primarily Holmesimysis costata, as food for
86 E. V. THUESEN AND J. J. CHILDRESS
up to 48 h after capture. They were then held without mollis, and Leukartiara octona, were measured at 15C
food for 24 h until their manubria were empty, before following the latter method. The oxygen consumption
being frozen for enzyme activity investigations. Selected ratesofacclimated L. octonaweremeasuredat 5C. Oxy-
individuals of L. octona were acclimated to a colder gen consumption rates at 10C ofPeriphylla periphylla
temperature. 5C. in a planktonkreisel for 1 week under and Colobenema sericeum were measured with oxygen
the same food conditions and then used for respiration electrodes.
experiments. Control syringes offiltered seawatercontainingthean-
Some specimens that were originally frozen in liquid tibiotic mixture but without animals were run simulta-
nitrogen were stored up to 6 months in a 80C freezer neously. After removal ofthe animals, syringe and res-
without detectable loss of enzyme activities. Animals pirometer experiments were periodically left to continue
collected by meter net and remotely operated vehicle, ascontrolstocheck forbacterialcontamination. Ifpresent,
without thermal protection, were used only for enzyme background respiration was subtracted from animal res-
assay investigations. piration. Background respiration was always undetectable
The report on the hydromedusae of the Indian and at 5C. After experiments at sea, animals were weighed
Pacific Oceans by Kramp (1968), Russell's treatises on using a shipboard motion-compensated precision balance
Atlantic medusae (Russell, 1953, 1970) and the numerous system (Childress and Mickel, 1980). In the laboratory,
references cited therein were indispensable in our iden- animals were weighed on an analytical balance. All spec-
tification ofmedusae to species. imensused inoxygenconsumption experimentswerelater
frozen in liquid nitrogen for spectrophotometric analysis
Metabolic rate measurement ofenzyme activities.
Oxygen consumption measurements on animals that Biochemical analysis
were recovered in excellent condition were carried out
either on board ship or in the laboratory. Our previous The following enzymes were screened to select appro-
experiments on the effect ofhydrostatic pressure on two priate indicators ofaerobic and anaerobic metabolic po-
bathypelagic hydromedusae, Crossota rufobrimnea and tential: citrate synthase (CS, E.C. 4.1.3.7), malate dehy-
Aegina citrea. showed no significant differences in met- drogenase (MDH, E.C. 1.1.1.37), lactate dehydrogenase
abolic rates measured at 1 and 101 atm (Childress and (LDH, E.C. 1.1.1.27), pyruvatekinase(PK, E.C. 2.7.1.40),
Thuesen, 1993). Therefore, all metabolic rates were octopine dehydrogenase (E.C. 1.5.1.11), alanopine de-
measured at atmospheric pressure. Oxygen consumption hydrogenase (E.C. 1.5.1.17), and strombine dehydroge-
rates were measured in two ways, depending on the size nase(E.C. 1.5.1.?). Although weassayed fortheseenzymes
ofthe animal. Larger animalswere transferred to water- in a variety of medusae, our study focused on CS and
jacketed respiration chambers of appropriate size con- LDH as two enzymes representative ofmetabolic poten-
taining 5C filtered seawater with antibiotics (0.20-/jm tial. CS isan important regulatory enzyme and functions
MDH
membrane filter; 25 rngT1 each of streptomycin and inthefirststepofthecitricacidcycle. playsavariety
penicillin) and equipped with small stirring pumps con- ofroles in intermediary metabolism and is important in
sisting ofa magnetic stirring bar enclosed within a dis- thecitric acid cycle. These enzymes serveasindicators of
LDH
creteplasticchamber. This mechanism allowed forgentle aerobic metabolic potential. istheterminal enzyme
mixing of water and provided sufficient flow for the in glycolysis, and PK is the regulatory enzyme that sup-
LDH
Clarke-typeoxygen electrodes(Mickel el a/., 1983)with- plies pyruvate for in the second-to-last step in gly-
out damage to the animal. Smaller animals were trans- colysis. Thesetwoenzymesareexcellent indicatorsofgly-
ferred to glass syringes used as miniature respiration colytic potential and contribute to both aerobic and an-
chambers (Thuesen and Childress, 1993a). The syringes aerobic metabolic pathways. Becausewedid notassaythe
with filled with filtered seawater containing antibiotics various opine dehydrogenase in all the species in this
as above and incubated at 5C. Periodically, a gas-tight study, it could be that one or more ofthese enzymes are
syringe was used to withdraw water samples from the betterindicatorsthan LDH ofanaerobicpotential in some
incubation syringe through a three-way valve, and the species. CS, MDH, LDH. and PK activitiesin fish muscle
new incubation volume was noted. Before the sample have all been found to correlate well with oxygen con-
was withdrawn, syringes were turned end-over-end sev- sumption rates (Childressand Somero, 1979; Somero and
eral times to mix the incubation medium. Oxygen and Childress, 1990; Sullivan and Somero, 1980; Torres and
carbon dioxide content ofthe water was measured with Somero, 1988).
a gas chromatograph (Childress el a/.. 1984). Whole animals were weighed on a Mettler analytical
Oxygen consumption rates ofhydromedusae from the balancewhiletheywerestill frozenandwerehomogenized
Santa Barbara Channel. Vallentinia adherens. Eirene ataverylowdilution (from 1:1 to 1:9partsweight/volume
METABOLIC CHARACTERISTICS OF CALIFORNIA MEDUSAE 87
M
in 0.01 A/Tris homogenization buffer, pH 7.5, at 10C) sured at sea. Frozen tissue was homogenized in 0.1
in Duall hand-held glass homogenizers kept on ice. Low perchloricacid, neutralized toa pH of 10with KOH, and
dilutions were used to detect the low enzyme activities centrifugedat6600 Xgfor 10 min. Lactateconcentrations
presentin medusan homogenates. Very largeanimalswere in the supernatant were measured enzymatically using L-
subsampled by removing a wedge-shaped piece of the lactic acid assay reagents (Boehringer-Mannheim).
whole animal for homogenization. Aliquots of homoge-
nate were transferred to microfuge tubes and ccntrifuged Statisticalanalysis
at 6600 Xgfor 5 minat 5C. Unliketheenzymeactivities
of fish muscle, activities in whole-animal homogenates All statistical analyses were performed with Statview II
decreasedby20-40%after4 h standingon ice. Therefore, orSuperANOVA (AbacusConcepts, Inc., Berkeley, CA).
all assays were performed within 1 h ofhomogenization, Simple linear regressions, multiple regressions, Kendall
usinga Shimadzu UV160U spectrophotometerequipped nonparametric rank correlations, and analysis ofcovari-
with a water-jacketed cuvette holder. The subumbrellar, ance (ANCOVA) were used to explore the relationships
orswimming, muscle ofsome ofthe largerspeciesofme- among the parameters that were measured in this study.
dusae was readily excised. For these species, the enzyme Simple linear regressions were used to describe the rela-
activities in these muscles were also measured. Small tionships between various variables, including relation-
amounts of sample supernatant (10, 25, or 50 ^0 were shipsbetween weight-specificcitratesynthaseactivityand
used for assays. To estimate maximum metabolic poten- weight-specific metabolic rates. Regressions oftotal (not
tial, measurements ofenzyme activity were made in 1- standardized by weight) CS activities versustotal oxygen
ml quartzcuvettesat 20C under nonlimitingconditions consumption rateswere not used. Although this statistical
and followed proceduresessentially the same asthosede- methodology has been used in previous studies on zoo-
scribed previously (Childress and Somero, 1979; Somero plankton physiology, itessentiallyregressesbodymasson
and Childress, 1980). Enzyme activities are expressed as the r-axis with body mass on the .Y-axis, and it thereby
units(micromolessubstrateconverted toproduct permin) results in higher values ofcorrelation coefficients and ap-
per gram wet weight ofanimal. parent statistical significance when compared with a slope
CS activity was measured in a medium containminMg ofzero. It does not, however, testthe relationship between
50 mAI imidazole/HCl buffer (pH 7.8 at 20C), 0.5 enzyme activity and oxygen consumption rate indepen-
mM mM
oxaloacetate, 0.1 acetyl-CoA, 0.1 5,5-dithiobis dent ofbody size. All rates ofoxygen consumption and
mM
(2-nitrobenzoic acid) (DTNB), and 1.5 MgCl:. The enzyme activity referred to in this study are weight-spe-
increase in absorbance at 412 nm due to the reaction of cific. All the regressions in this study were carried out on
the reduced coenzyme A generated by the enzymatic re- In-transformed data to improve linearity.
action with DTNBwasrecorded. Background activitybe- Oxygen consumption rates and enzyme activities of
fore the addition of homogenate supernatant was re- medusae were evaluated in relation to wet mass of the
corded,andthisbackground ratewasthensubtracted from animals, and scaling coefficients from the allometric
the overall rate after the assay reaction was initiated by equation v = aMhwerederived, where A/isthewetweight
addition of the oxaloacetate. Background activity was ofthe animal, b is the scaling coefficient, and a is a con-
subtracted from total activity to calculate the enzyme ac- stant for the species at a given temperature (Schmidt-
tivity ofthe sample. MDH activity measurements were Nielsen, 1983). Mean values ofspecificoxygen consump-
performed in a medium containing 100mA/ Tris/HCl tion rates and the enzyme activities ofwhole-animal ho-
mM mM
buffer (pH 8.1 at 20C). 20 MgCl2, 0.4 oxalo- mogenates foreach specieswere used in comparisonswith
acetate, and 150/nA/NADH. LDH activitywasmeasured crustacean and fish data from the same region (metabolic
in a medium containing 80 mA/Tris/HCl buffer(pH 7.2 ratedataon pelagiccrustaceans [Childress. 1975] anden-
at 20C), 2 mM sodium pyruvate, 150 nM NADH, and zyme activities of fishes [Childress and Somero, 1979;
100 mM KC1. PK activity was measured in a medium Wells and Childress, unpublished]) using ANCOVA to
containing 50mA/ imidazole/HCl buffer (pH 7.8 at testwhethertheslopesofthevariousrelationshipsbetween
20C). 100 mA/ KC1. 10 mA/ MgSO4, 0.1 mA/ fructose- minimum depth of occurrence (MDO) and enzyme ac-
bisphosphate. 1.0mA/ phosphoenolpyruvate, 5.0mA/ tivity were significantly different. The Kendall rank cor-
ADP, 150 n\f NADH and excess LDH activity (rabbit relation was used to test for significant relationships be-
MDO
muscle LDH, Sigma Chemical Co.). The assay reactions tween and the biochemical-physiological parame-
of MDH. LDH. and PK were started by addition ofthe ters without any assumptions ofform or linearity ofthe
sample supernatant, and the decrease in absorbance at relationships and to find correlations between the bio-
340 nm due to NADH oxidation was recorded. chemical and physiological data. Sincethesetestsareper-
Lactateconcentration intentacleandswimming muscle formed on data from within a single region that has a
tissueofPeriphyllaperiphyllaandAeginacitreawasmea- consistent relationship between temperature and depth.
88 E. V. THUESEN AND J. J. CHILDRESS
no correction for temperature difference is necessary. Analysis of all individuals of all species of medusae
MDO in a given region is defined as that depth below showed the familiar pattern of decreasing oxygen con-
which 90% ofthe population usually can be found (Chil- sumption rate with increasing wet weight ofanimals at
dress, 1975). A depth of 10 m wastaken asthe MDO for both 5 and 15C (Fig. 1). Scyphozoans analyzed as a
animals living at 10m or shallower to avoid distortions separate group also showed a highly significant relation-
in regressions of In-transformed data. Medusan MDOs ship between size and metabolic rate (b = -0.26; Ftest
are based on ourpersonal observations usingthe opening- forregressioncoefficient, P<0.01, 95%CI: 0.17). How-
closing Mother Tucker trawl and published bathymetric ever, among the hydrozoan medusae there was a less sig-
distributions ofmedusae offsouthern California (Alvar- nificant effect ofsize on metabolic rate (b = -0.13; Ftest
ino, 1967). When we did not have sufficient data to eval- for regression coefficient, P = 0.07, 90% CI: 0.1 1). Al-
uateMDOforagiven species,theshallowestcapturedepth though analysis ofmost species over a large enough size
was used. This was only done forthe rarerspecies ofme- rangewith asufficient number ofindividualstodetermine
dusae, whichwere uncommonly captured in trawls. Min- species-specific scaling patterns was not possible, it was
imum capture depths for Tiaranna rotunda, Euphysora undertaken forAegina citrea, Crossota rufobrunnea, and
gigantea. and Neoturrisfontata are 650, 350, and 650 m, Penphylla periphylla. A significant size-metabolism re-
respectively. The epiphytic medusa I". adherens was ex- lationship was found only for C. rufobrunnea. which had
cluded from depth comparisons ofpelagic species. a scaling coefficient of -0.31 (Ftest for regression coef-
Wet mass was used as the size measurement, because ficient, P = 0.02; 95% CI: 0.25).
this parameter is the physiologically significant one that
determines constraints on animal locomotion, behavior, Enzyme activity
etc. Other measurements, such as dry weight or protein
content, used as indicators ofsize can lead to misinter- Citrate synthase, lactate dehydrogenase. pyruvate ki-
pretationsconcerningthebiologyandecologyofthewhole nase, or malate dehydrogenase activities were measured
organism. The significance of using various parameters on more than 150 individuals of32 species of medusae
ofbody size in this regard has been discussed previously (Table II). LDH and CS activities were measured in iso-
(Childress, 1977; Childress and Somero, 1979). lated swimming muscle oflarge medusae: Pelagia color-
ata. Atolla wyvillei, Periphyllaperiphylla, and Solmissus
Results incisa (Table II). We could not detect octopine dehydro-
genase in any species tested (whole-animal homogenates
Oxygen consumption measurement ofPelagia colorata. AitreUa aurita, an unidentified epi-
Many species of medusae were collected in excellent pelagic hydromedusan, Crossota rufobrunnea, Crossota
condition by using the large insulated cod end. These in- alba, Haliscera conica, Haliscera bigelowi, or isolated
cluded four undescribed species ofTrachymedusae: Pan- muscle of P. colorata and P. periphylla). We also could
lachogonsp. A(cf.P. haekeli). I'ampyroerossotachildressi not detect either alanopine dehydrogenase or strombine
(Thuesen. 1993), Tetrorchis sp. A (distinct from T. ery- dehydrogenase in any species tested (whole-animal ho-
ihrogaster), and an orange and pink rhopalonematid. mogenates ofC rufobrunnea, C. alba, H. conica, andH.
Crossota sp. A. Very large and fragile animals, such as bigelowi or isolated muscle ofP. periphylla).
Solmissus incisa, could not be collected in sufficiently ThehighestCSactivitiesweremeasured intheepiphytic
healthy condition foroxygen consumption rate measure- medusa I'allentiniaadherens. Thehighest LDH activities
ments; however, smaller fragile animals, such as species weremeasured inP.periphylla. Citratesynthaseand LDH
ofthe Halicreatidae, were often collected with tentacles activities in 5. incisa were lower than could be detected,
more than several body-heights in length and with intact but both these enzymes were measured at low levels in
swimming bells. These animals were still swimmingafter isolated swimming bell muscle. Citrate synthase could not
24 h in the incubation syringes. Coronate medusae, rho- be detected in whole-animal homogenates or in isolated
palonematids, and other robust animals were caught in coronal muscle ofA. wyvilleiandA. vanhoeffeni. although
pristine condition and could be maintained alive and the coronate medusae ofother genera had readily mea-
swimming for several days in 20-1 buckets in a 5C re- surable CS activities. CS activity was higher than LDH
LDH
frigerator. Oxygen consumption rates were measured on activity in many ofthe species, although Hactivities
14 hydrozoansand 5 speciesofcoronate scyphozoan me- were higher than CS activities in A. citrea. maasi.
dusae; mean rates are presented in Table I. Oxygen con- Ptychogena lactea. and the coronate scyphozoansA. van-
sumption ratesofthreespeciesofmedusaewere measured hoeffeni, A. wyvillei, P. periphylla, and Nausithoe rubra.
at two temperatures, and the Q, for Leukartiara octona PK and MDH activities were usually higher with respect
and the estimated Q values for Colohenema sericeum to their corresponding LDH and CS activities in the few
10
and Penphyllaperiphyllaare 3.5,4.8.and2.6,respectively. species for which these enzymes were investigated; how-
METABOLIC CHARACTERISTICS OF CALIFORNIA MEDUSAE 89
Table I
Metabolicratesol'medusaecollectedoffCalifornia
Class
Order
Family
Genusand species
90 E. V. THUESEN AND J. J. CHILDRESS
medusan oxygen consumption rate with depth is signifi-
cantly different from that observed for pelagic crustaceans
(ANCOVA, P < 0.02; Fig. 5). The variation in CS activ-
itieswith depth ofoccurrence in medusae (both with and
without I'. adherens data) is significantly different from
the observed decrease in CS activity for pelagic fishes
0.1- (ANCOVA, P < 0.02; Fig. 6A). The variation in LDH
activities with depth in pelagic medusae is significantly
different from thatobserved forpelagic fishes(ANCOVA,
60 P< 0.004; Fig. 6B). Kendall's nonparametric testofrank
correlation failed to show any significant correlation of
0.01 mean medusan metabolic rate or enzyme activity with
0.01 0.1 10 100 minimum depth ofoccurrence.
10n
f Discussion
crt
3 I'ariahilitv
g Using an elaborate respirometer and a painstaking
OX method of chemical analysis to determine oxygen and
carbon dioxide content, Vernon (1895) was the first to
measure the oxygen consumption rates of medusae. He
observedconsiderable variabilityand, forthescyphozoan
Rhiiostomapulmo, noted "distinct differences in the res-
piratory activity of different individual medusae" that
0.1 could not be explained by size effects. Otherinvestigators
0.01 0.1 have also shown high variability in metabolic rate mea-
Mass (g) surementsofgelatinousanimals(e.g.. Biggs, 1977; Larson,
Figure 1. Oxygen consumption rates at 5C (A) and 15C (B) of 1987b). Oneexplanation maybethatthe nutritionalstatus
California medusae as a function oftheir wet weight. The slope ofthe of the organism is reflected in metabolic rate measure-
regression line for 5C experiments is v = 0.141 .v 22: R = 0.45. The ments. Medusae undergo rapid periods of growth with
slopeofthe regression line for 15Cexperiments isy = 0.712 .v~-26: R high food concentration; furthermore, they "degrow"
c=Vrael0al.te7in7dt.aienSiya(mab)do,hlResrheofnposral(aoAn)ni.emmaLaletspitadoraemeeads(u+sf)oa.lelCoo(wrs:o),nNaLait'reicioskumcryetpdiahurosamaoeecdlu(o5s3n)aa,e(HAa()lO.i).- bdlueriangmipneiraitoudrseofadsutlatrv(atHiaomnnaenrdadnecdreJaesnessienn,siz1e97to4)r.esAerma-i
(1986) manipulated the nutritional status of the hydro-
zoan Aeqitorea victoria and observed higher metabolic
P < 0.05 for both regressions). Correlation coefficients rates in animals that had been starved for 3 days. She
were significant, P < 0.05 for both regressions, with R = concluded that this was not due to behavioral changes
0.31 and 0.63 in the 5 and 15C analyses, respectively. and was unabletoexplain herfindings. Otherinvestigators
have shown that nutritional status can be reflected in the
Respiratory rate andenzyme activity in relation to enzymeactivitiesofsomeorganismswithindaystoweeks
depth ofoccurrence (Bamstedt, 1980; Clarke et a!.. 1992; Clarke and Walsh,
1993; Lowery et a/.. 1987; Roche-Mayzaud et ai. 1991).
No significant decline in metabolic rate or enzyme ac- It is unknown how quickly enzyme activities in medusae
tivity can be ascribed to minimum depth ofoccurrence are influenced by nutritional status.
in pelagic medusae (Figs. 5 and 6). The slopes ofthese Our investigation ofenzymatic scaling in the demersal
regressions are not different from zero at the 95% signif- jellyfish Polyorchispenicillatususedindividualsthatwere
icance level. handled differently than other animals in this study, and
The slopes ofthe regressions describing the variation the results ofthese experiments are less variable than re-
in metabolic rates and enzyme activities with depth are sults for the other species investigated. These Polyorchis
not statisticallydifferent from zero: however, theyare sig- had been kept in a planktonkreisel for up to 24 h with
nificantly different from those forothergroups that show high concentrations of food. Perhaps the more uniform
significant declines in metabolic rates and enzyme activ- nutritional status of these individuals reduced the vari-
ities with depth ofoccurrence. The pattern ofchange in ability oftheir enzyme activity.
METABOLIC CHARACTERISTICS OF CALIFORNIA MEDUSAE 91
Table II
l-'n:\incactivities<>JCaliforniamedusaemeasuredat 20C
Class
Family
Genusandspecies
92 E. V. THUESEN AND J. J. CHILDRESS
10
w>
~ o
60 o
D 1 a-,
C 0.1
J
5, 0.01 -, 0.01
VJ
s
-a
2 0.001 - u 0.001
U 08
O
(3
10-i"-4 io-4
4 4
0.001 0.01 0.1 1 10 100 1000 IO 0.001 0.01 0.1 1 10 100 1000 IO
Mass (g) Mass (g)
Figure 2. Citrate synthase activity as a function ofwet weight for Figure-3. Lactatedehydrogenaseactivityasafunctionofwetweight
California medusae. The slope ofthe regression line is r = 0.066.V" '"; forCaliforniamedusae.SymbolsformedusaearegiveninFigures 1 and
R = 0.67. Symbols formedusaearegiven in Figure I. andalsoinclude 2. Theslope ofthe regression lineisy = 0.027.v"; R = 0.08.
Polyorcliispenicillatus(D)andotherscyphomedusae().
skeletal muscle ofsome ofthe deeper-living teleost fish,
and most likely are active swimmers. Some ofthe species
This investigation included one species of "benthic" that have very low metabolic potentials are probably sit-
medusa: I'allentinia adherens. In contrast to the pelagic and-wait predators maintaining theirposition in thewater
lifestyle of most medusae, I". adherens lives attached to column with only periodic contractionsofthe swimming
kelp frondsand isexposed to much movemenWteand water bell. Laterally flattened, or disk-shaped, medusae have
turbulence as it maintains itselfnear shore. interpret lower CS activities than dorsoventrally elongated medu-
the high CS activities in I'. adherens as an indication of sae, indicatingthat morehydrodynamic formshavehigher
a metabolically robust animal that is adapted to life in metabolic potentials (for example, compare the more
such a high-energy environment. Thus, we believe that streamlined Rhopalonematidae with the Halicreatidae in
theinterspecific variabilityofenzymeactivitiesintheme- Table
II).
dusae investigated in this study indicates different phys-
iologicaladaptationstotheirenvironments. Forexample. Enzymes
Pelagia colorata and Periphyllaperiphylla have LDH ac- Some invertebrates useoneor moreamino acidsasthe
tivities in swimming muscle comparable to those ofthe terminal acceptor in glycolysis (Hochachka and Somero,
Table III
AlhiHcinc \culingrelationships ofen:ynitincactivitiesofpelagicmedusaefrom California
Enzymatic activityg ' wet weight (r)asa function oftotal body wet
weight (.1/1, y = aMh
Group
METABOLIC CHARACTERISTICS OF CALIFORNIA MEDUSAE 93
00
o o o
cP
o
I
H. sO O
|
O
1 o
8
I
X
o
0.01
0.001 0.01 0.1
Citrate synthase activity (units g' )
60
o
o
s.