Table Of ContentReference: Biol. Bull 187: 348-407. (December. 1994)
Metabolism and Amino Acid Transport
Energy
During Early Development of Antarctic
and Temperate Echinoderms
FRASER M. SHILLING1 AND DONAL T. MANAHAN2
Department ofBiological Sciences, University ofSouthern California, LosAngeles,
90089-0371
California
Abstract. Theratesofoxygenconsumptionbyembryos Introduction
ofantarctic echinoderms (Acodontaster hodgsoni, Odon- Manyspeciesofmarineinvertebratesin Antarcticahave
taster validus, Psi/asler charcoti. and Sterechinus neu- lecithotrophic (nonfeeding) stages ofdevelopment (Pearse
maveri) were compared to the biomass (ash-free dry or- etui. 1991). Forantarcticspeciesthathaveplanktotrophic
ganic weight) of the egg of each species. These species (particle-feeding) larvae, the strategies for survival in a
could survive for months to years (range: 10 months to low-food environment remain unknown. For example,
5 years) by relying solely on the reserves present in the Odontaster validus is a very abundant echinoderm (as-
egg. However, certain speciesdid not use any ofthe egg's teroid) in McMurdo Sound, Antarctica, and hasa plank-
reserves during early development. Embryonic stages of totrophic larval stage (Pearse. 1969). The adultsspawn in
O. validus (a species with planktotrophic larvae) did not austral winter (June-September: Pearse et a/., 1991) and
decrease in lipid, protein, ortotal biomassduringthe first larvae are present for several months in a water column
35 days of development. During the first 42 days of that has very low concentrations of phytoplankton (ca.
development, embryos of A. hodgsoni (a species with 0.01 Mg chlorophyll a I'1, Rivkin, 1991). Yet, when cul-
lecithotrophic development) used protein as an energy tured in situ in the water column, larvae ofthis species
source. Forboth species lipid composed 40 to 50% ofegg survive for weeks to months (Olson et ai. 1987) prior to
biomass, but was not used as an energy reserve. Larvae thephytoplankton bloom ofaustral summer(December-
of O. validus have a high-affinity transport system for January, Rivkin, 1991).
=
amino acids dissolved in seawater (K, 1.3 tiM for ala- The present study was undertaken to determine the
nine). The rate ofalanine transport from a low concen- physiological bases for the survival of antarctic echino-
tration (50 nM)could supply 32% ofthe larva's metabolic derm larvaelivingunderlow-foodconditions. Ithasbeen
needs. This is a 10-fold higher input to metabolism than suggested that, inthe near-absence ofalgae, larvae ofant-
was determined (3% at 50 nM) for larvae ofa temperate arctic echinoderms could be using other sources offood,
asteroid, Asterina minima. Larvae of antarctic echino- such as bacteria ororganic material dissolved in seawater
derms live in an environment where the food supply is (Rivkin et ai, 1986). In addition, larvaecouldbeendowed
low formosi heyear. Relativetotheir metabolic rates, with large amounts ofenergy reserves from the egg. This
antarctic larva^ 'me larger energy stores and plankto- would permit survival in a nutrient-poor water column
trophic larvae haw higher nutrient transport capacities ifthe larvae have lowermetabolic rates(cf.temperate lar-
when compared to larvae from temperate regions. These val forms) and correspondingly lower rates ofutilization
physiological differences allow antarctic larvae to survive of energy reserves. In the present study, egg mass and
for long periods without particulate food. metabolic rateswere measured forfourspeciesofantarctic
echinoderms to allow for a calculation oflife span in the
Received 4June 1993;accepted 2t> September 1994. absence ofany exogenous food source. Embryos ofAco-
Ore:'gCAuodrndrreHenestaslatfdohdrrSecscosir:ernVecoseplsolnUundmievnIecnrsest.iittuyt.eLf-or47A4d,vaPnorcteldanBdi.omOeRdic9a7l20R1e.search, odopnmteanstt)erahnoddgOs.onvial(iadusspewceirees awlistohcluelctiutrheodtrtohprhoiucgdheveeml--
398
ENERGETICS AND NUTRIENT TRANSPORT 399
bryogenesistodetermineactual ratesofutilization ofbio- and concentrated ontoa nylon screen (80 ^m, mesh size)
mass (ash-free dry organic weight) and energy reserves that was partially immersed in ambient seawater. At each
(lipid and protein content). To assess the possible role of change of seawater, three to six samples were taken for
dissolved organic material asasource ofnutrition forlar- the measurement ofbiomass (ash-free dry organic weight)
vae, the mass-specific rates ofamino acid transport from and an additional three samples were taken forbiochem-
seawaterwerecompared with the mass-specific metabolic ical composition (lipid and protein content). Salts were
rates of larvae. These physiological processes (amino removed from the samples using serial washes ofan am-
acid transport and metabolic rate) were measured for monium formate solution (methodsdescribed previously
larvae ofO. validus and compared to the measurements by Jaeckle and Manahan, 1989). Protein content was
made for similar larvae ofa temperate asteroid (Asterina measured with the Bradfordassay(1976). Trichloroacetic
miniata). acid-insoluble protein was dissolved by heating (60C)
theprotein pellet in 1 A/NaOH (aq.). Thismethodresults
Materials and Methods in a close (7%) approximation ofthe absolute amount of
Culturing ojembryos andlarvae pmraontecien,liaqsuiddectherromminaetdogbryapmheyatshueritnotgalwaitmhinhoigahc-ipdercfoonr--
Adult echinoderms were collected using scuba from tent of acid-hydrolyzed protein homogenates of larvae
several locations in McMurdo Sound, Antarctica, during (Manahan el a/., unpub. obs.). Lipid was measured ac-
austral spring (asteroids: Acodontaster hodgsoni, Odont- cordingto Mann andGallager(1985). Carbohydratecon-
aster validus, Perknasterfuscus, Psilaster charcoti; and tentwasnotmeasured inourstudiesbecausecarbohydrate
theechinoid, Sterechinusneumayeri). Priorto spawning, is a low percentage (2-4%) ofthe total organic material
adultswere maintainedinambientseawater(onseatables) ineggsofantarcticechinoderms(McClintockand Pearse,
for up to 2 weeks in the aquarium at McMurdo Station. 1986), as has been reported for eggs and larvae ofother
Gametes were obtained from adult asteroids by intracoe- species ofmarine invertebrate (Holland, 1978).
lomic injection of 1 mA/ 1-methyladenine. Gametes from
0s.e5a uMrchKiGn.s wFeerrteiloibzteadinegegdsboyfitnhteraanctoaerlcotmiiccsipnejceicetsiowneroef Metabolic rates ojembryos and larvae
suspended in 200-1 vessels (Nalgene) offiltered seawater Rates of oxygen consumption were measured using
(0.2jim pore-size). Eggs(andlatertheembryosand larvae) Strathkelvin (Glasgow, U.K.) polarographic oxygen sen-
were kept in suspension by mixing the cultures with ver- sors (Model 1302) that were connected to oxygen meters
tically moving Plexiglas paddlesdrivenbyelectric motors (Model 781 ). The output (as volts) from each meter was
set at slow speeds (5-10 rpm). Low concentrations ofin- recorded by an IBM computer using a software package
dividuals were maintained in the culture vessels (e.g., O. fordataacquisition andanalysis(Datacan, Sable Systems
mr
validuswasculturedat 2-3 individuals 1 andA. hodg- Inc., Los Angeles, California). Two or three respiration
soniat 0.1 individuals mr1). The temperature ofthe cul- chambers (Strathkelvin, Model RC 200) were used si-
tureswas maintained by immersingthe 200-1 culture ves- multaneously and two to six independent measurements
sels in tanks offlowing ambient seawater (mean temper- ofrespiration weremadeusingdifferentgroupsofembryos
ature of-1.2C). The culture seawaterwasreplaced every or larvae at the same stage ofdevelopment.
4 to 5 days with newly filtered seawater, at which time Rates ofoxygen consumption were measured for the
the vessels were cleaned by acid-washing. For O. validus, antarctic species at either -1.4C or -2.0C (see Results
one batch of eggs (a total of 1.5 million eggs obtained forcorresponding temperature and experiment). Oxygen
from several females) was divided equally among three consumption wasmeasured onthesamedaythatsamples
replicate 200-1 culture vesselsto ensure sufficient numbers were taken forbiomass and biochemical composition, or
ofindividualsin each vessel formeasurementsofbiomass, when rates ofalanine transport were determined. Prior
biochemical composition, and metabolic rates. Embryos to any series ofmeasurements on a given day, the respi-
and larvae of the temperate species (Asterina miniata) ration chamber and the membrane ofthe oxygen sensor
were cultured in California at 14C. Gametes ofthis spe- were washed with 75% ethanol to minimize bacterial ac-
cieswere obtained from ripe adults purchased from Mar- tivity, and then rinsed four times with filtered seawater.
inus Inc., Long Beach, California. At temperatures of -1.4 or -2.0C, the oxygen sensors
tookan averageof2-3 htostabilizewhen filtered seawater
Biochemical composition ofantarctic eggs (4 species) (with no animals added) was present in the respiration
andchanges in biomass during early development chamber. Toobtain reliable datafortheantarcticspecies,
ofA. hodgsoni andO. validus all respiration rates were determined only when at least
Prior to sampling, all ofthe embryos or larvae from a 2 h had elapsed after the animals were placed into the
singleculturewere slowlysiphoned from theculture vessel respiration chamber. Rates of oxygen consumption for
400 F. M. SHILLING AND D. T. MANAHAN
(A) O.validus (B) S. neumayeri
6
ENERGETICS AND NUTRIENT TRANSPORT 401
ing was recorded from the oxygen sensor placed in each in metabolic rate (Fig. 1C). However for P. charcoti, a
BOD
bottle containing reduced oxygen and the actual species with lecithotrophic development, no significant
amount ofoxygen present in each seawater sample was change was measured in metabolic rateduringthe period
then measured chemically with Winkler's titration. The ofdevelopment studied(to 32days)(Fig. ID, VR = 4.56ns,
decrease in theoxygencontentofseawatermeasuredwith ^o.o5[i.io] = 4.96). The lack ofstatistical significance may
the sensors was not significantly different from the de- be an effect ofa smaller sample size for this species.
crease as measured independently by Winkler's titration The metabolic rates ofthe bipinnaria larvae used for
(least-squares linear regression analysis, variance ratio of the comparison ofmetabolic rates and amino acid trans-
slope = 0.35ns, n = 7). port rates were 27.5 1.51 pmol O2 larva"' IT1 (n = 6)
for 5-day-old larvae of A. miniata (measured at 12C)
Measurement ofalanine transport rates by antarctic and and 2.22 0.69 pmol larva'1 h"1 (n = 4) for 42-day-old
temperate larvae larvae of0. validus(-2C). These differentagesoflarvae
for the two species represent the same stage ofdevelop-
Time course experiments were done at a range ofdif- ment(earlybipinnaria)becauseoftheslowerdevelopment
ferent alanine concentrations to determine the kinetics
of amino acid transport by larvae of O validus (at raantde otfhr0.ouvgahloiudtustrheilsatpiavpeetroA(.unmliesnsiaottah.eErrwriosressgtiavteend)hearree
-2.0C) andA. miniata(at 12.0C) (methodspreviously one standard error ofthe mean (1 SEM).
described by Manahan ct ai. 1989). Radioactive alanine
(3H-alanine, 84 Ci mmol"1. New England Nuclear) was Scaling ofmetabolic rates with biomass during early
added (2 or 5 /*Ci) to 10 ml ofseawater in the presence development ojantarctic echinoderms
of a range of concentrations (0.1-100 fiM) of nonra-
dioactive alanine (Sigma Chemical Co.). Aliquots (500 /ul) The scaling of metabolic rate to ash-free dry organic
containing larvae (O. validus: 222 ml"1 A. miniata: weight (biomass) forembryosotS. neumayeri, O. validus,
;
322 ml"1) weretaken from the 10-ml vial every2 min for A. hodgsoni, andP. charcotiisshown in Figure 2A. When
20 min. The transport rate ofalanine at a given concen- the logofmetabolic rate (mean ofall values foreach spe-
tration wascalculated (as pmol alanine larva"' h~') using cies from Fig. 1) was plotted against the log of biomass
(1)the measured rateofaccumulation ofradioactivity(as (mean for each species), a slope of 0.66 0.213 (95%
disintegrations per minute after quench correction), (2) confidence limit) was calculated. These metabolic data
the specific activity ofthe radiolabel, and (3) the number can be described by the power function:
of larvae per sample. The rate of alanine transport per Metabolic rate = 3.14M -66
larva as a function of increasing alanine concentration
was plotted to determine the affinity (K,) and maximum where metabolic rate isgiven aspmol CK individual"' h~'
capacity (Jmax) ofthe amino acid transporter in antarctic and mass (M) has unitsofngash-free dry organic weight.
and temperate larvae.
I'olume to biomass relationship, andlipidandprotein
Results content ofeggs ofantarctic echinoderms
Metabolic rates during early development The slope ofthe line describing the relationship ofegg
biomass to egg volume is 0.917 (Fig. 2B). The egg di-
Duringearlydevelopment of0. validus, from thebias- ameters for the five species used in this comparison were
tula (8 days) to late gastrula stage (27 days), there was an obtained from the following reports: S. neumayeri from
increase in metabolic rate (Fig. 1A) measured at -1.4C. Bosch elal. (1987), andA. hodgsoni, O. validus, P.fuscus,
The significance of this increase was determined using and P. charcotifrom Bosch and Pearse(1990). Values for
analysisofvarianceforthedataduringthat 19-dayperiod biomass and egg diameters used to construct Figure 2B
(variance ratio, VR = 6.80*. F005[i.23] = 4.28). The data are given in Table IA for fourofthe five species (egg vol-
for early bipinnaria (after 27 days) were not used in this umes based on a sphere). The data point for the eggs of
analysisofearlydevelopment because the increase in res- P. fuscus is based on the following values: biomass
prieraacthieodn. FraotreSd.indenuomtayceorniti(nFiuge. o1nB)c,etthhereelwaravsalanstiangcerewaasse X= 8170.~93 mm1.30.7 fig, diameter = 1200 /urn, volume = 904.7
in metabolic rate(VR = 8.28*, FO.O.MUS] = 4.54)from the The percent ofthe ash-free dry organic weight ofeggs
unhatched blastula(4days)tothegastrulastage(19days). thatwascomposed oflipid and proteinwascalculated for
The larval stage of A. hodgsoni (a bilobed bipinnaria, four asteroid species (Fig. 2C). Eggs of O validus had
Bosch and Pearse, 1990) haddeveloped by 36days. From equal proportions of lipid and protein, whereas eggs of
the early embryo (8 days) to the larval stage (36 days) the three other species (all have lecithotrophic develop-
there was an increase (VR = 14.41***, /r005(i.24] = 4.26) ment) had a greater proportion ofbiomass as lipid. The
402 F. M. SHILLING AND D T. MANAHAN
percent recovery ofdryorganicweightaslipid and protein
ranged from 65% (P. charcoti) to 89% (P. fuscus) i.e., (A)
100
1 1 to 35% oftotal dry organic weight was not accounted
for by the lipid and protein content ofthe eggs. 50
25
Changes in biomass, lipid, andprotein content during O 10
early development ofO. validus andA., hodgsoni O
Q. 5
Embryos of O. validus in the three replicate cultures
2
had similarchanges in biomass, lipid, and protein content
from the egg (0 days) to early bipinnaria larva (35 days) 1 0.5 1 10 25 50 100
(Fig. 3A). As stated earlier, one batch of eggs obtained Dryorganicweight(pgembryo~1)
from several females was used to start all three of the
200-1 cultures. Biomass increased significantly (ANOVA. 100
VR = 83.13***, F = 4.32) from the egg (0 days) 50
.o5[i.2i|
to the early gastrula stage (pooled data for 9, 10, and 12 10 -
day-old) and thereafter remained fairly constant (i.e., no
significant difference between gastrula and early larval
stageatd 35, VR = 2.24ns,Fomi32] = 4.12). Theequation o
for the fitted curve through all the biomass data points is 0.1J
given inthefigure legend. Linearregression analyseswere 5 10 50 100 500 1000
usedtodeterminetheratesoflipidandprotein utilization Eggvolume(x10 3mm3 )
during early development ofO. validus (regression lines
excluded forgraphicalsimplicity. Fig. 3A). Lipidand pro- Protein
1
tein content did not change significantly (determined by D
ANOVA) from the egg to early larva (VRpmtein = 0.22ns, LiP'd
VR,,pld = 0.09ns, n = 22).
For the first 42 days of development ofA. hodgsoni,
lipid content did not change (Fig. 3B, VR = 0.0lns, n
= 25). Both protein content and biomass did, however,
decreaseduring this period. Protein decreased at a rateof
25.7 8.8 ng individual-' day'1 (VR = 8.60**. FOM[tM] Ah PC Pf
= 4.32). Biomass decreased at a rate of 52.4 14.3 ng
individual"1 d"1 (VR = 13.49**, F005[l:2i] = 4.28). (asFhi-gfruereed2r.y oMregtaanbioclwiecigshcta)li,nga,ndrellaiptiidonasnhidpporfoteegignvcoolnutmeenttoofbiegogmsasosf
antarcticechinoderms. Ah.Acodonlasterhodgsoni:Ov, Odontasterval-
Transport ofalaninefrom seawater bylarvae idus: PC, Psi/astercharcoti; Pf, Perknasterfuscus;Sn, Sterechinus neu-
of\. miniata andO. validus mayeri(echmoid,closedcircles).(A)Changeinmetabolicrateasafunc-
tionofembryos' biomass,errorbarsrepresent95%confidencelimitsof
The larvae ofA. miniata had a maximal transport ca- the mean, where no error bars are shown errors fell within graphical
pacity(JmaJforalanineof17.15 pmol Mg~' h'1 (at 12C), representationofdatapoint. (B)Relationshipofeggbiomasstoeggvol-
whereas the Jmax for alanine by larvae ofO validus was ume. (C) Lipid and protein content ofeggsas percent ofbiomasswith
6.51 pmol fig'1 hT1 (at -2C) (Fig. 4A). The affinities 95%confidence limits.
(values ofK,) ofthe alanine transport systems in larvae
ofboth speciesweresimilar(seeslopes. Fig. 4B), at 1.9 t
forA. miniata and 1.3 nM for O. validus. timate oflarval life span under starvation conditions can
beobtainedbycalculatinghow longthe maternal endow-
Discussion ment ofenergy reserves initially present in the egg could
Lifespan ofembryos andlarvae supplythe metabolicdemand(ratesofrespiration)ofem-
bryos and larvae. Starvation conditions are defined here
Antarcticechinoderm larvae havetosurvive periodsof as the absence ofany dietary inputs, either in paniculate
many monthsin a nutrient-poor watercolumn (Olson el form orasdissolvedorganicmaterial. Theenergyavailable
ai, 1987;Pearserta/., 1991;Rivkin, 1991). Survivalunder as biomass in the eggs ofspecies with planktotrophic and
such conditions should be difficult, especially for those lecithotrophic modes of development was compared to
species with larval forms that require food to complete the metabolic rates of those same species during early
development (e.g., O. validus and S. neumayeri). An es- development (Table I). The time it would take to deplete
ENERGETICS AND NUTRIENT TRANSPORT 403
Table I
Calculation o!thedurationof/anallifespan:(A)fartheantarcticechinodermsAcodontaster hodgsoni, Odontastervalidus, Psilastercharcoti,and
Sterechinusneumayeri. (B) FortemperateechinodermsAsterina miniataandSt.ongylocentrotus purpuratus
(A)Antarcticspecies:
Species O. validus S neumayeri A. hodgsoni P. charcoti
Eggsize' (Mm) 170 179 550 950
Eggbiomass2(Mg+ SEM) 0,63 0.018 0.69 0.032 30.1 0.06 81.3 1.91
Metabolic rate3(pmol O2 ind.-' IT') 2.94 +0.18 2.90 0.33 26.1+2.26 63.9 + 5.09
Biomassdepletion4(ngind."' day"') 1.08 1.06 9.55 23.4
Timetodeplete 50% ofeggbiomass(months) 9.8 10.8 52.5 58.0
(B)Temperate species:
Species A. miniata S purpuratus
Eggsize1 (jim)
404 F. M. SHILLING AND D. T. MANAHAN
Dryorganicweight
3.
"nDTO
Lipid&protein
O -
20
Age(days)
(B)
ENERGETICS AND NUTRIENT TRANSPORT 405
Table II
Mass-specificmetabolicratesandmass-specificratesofalaninetransportforbipmnaria lan'aeo/"Odontastervalidus(42-day-old) andAsterina
miniata (5-dav-old)
O. validus(-2C) A. miniata (12C)
Metabolic rate'
406 F. M. SHILLING AND D. T. MANAHAN
crease in lipid or protein content ofO. validusduringthe the "Winfly" period on the ice. Ourthanksalso go to Dr.
period ofbiomass increase. The biomass increase of O. John Pearse for discussions about conducting this re-
validus is probably not due to a gain in carbohydrate, as search. Antarctic Support Associates, The U.S. Navy
marine invertebrate eggs and embryos do not contain (VXE-6), and The National Science Foundation provided
much ofthis energy reserve (Holland, 1978; McClintock logisticand scientificsupport in Antarctica. Thisresearch
and Pearse, 1986; Jaeckle and Manahan, 1989; Shilling wassupported by NSFgrant 88-20130. One ofus(DTM)
and Manahan, 1990). An alternative explanation for the would like to dedicate this paper to his deceased father,
observed increase in biomass ofO. validus is that the in- the late Mr. C. A. Manahan.
crease is an artifact ofthe measurement techniques used
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Acknowledgments Manahan, D.T. 1990. Adaptationsbyinvertebratelarvaefornutrient
acquisition from seawater. Am. Zoo/. 30: 147-160.
We are most grateful to Dr. Isidro Bosch for his assis- Mann, R., and S. M. Gallager. 1985. Physiological and biochemical
tSaonucned,inaconldlefcotrinhgitsheasasnitsatracntciecewicthhinloadrevarlmscuilntuMrcinMgu.rWdeo McCe(lBniienvrtagloevtciikac,:sToJe.frlBea.dr,ivmaaednadoef)J.T.eJSr.edEPoxepna.arvsMaeal.ris.1L9B.8i6oal.n.dEBcOoarlng.kai8n5ai:cgo2a1unl1dd-i2e2(n8Bea.rrgtestcihc)
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