Table Of ContentReference:Biol. Bull. 192:262-278.(April, 1997)
Decline in Pelagic Cephalopod Metabolism With
Habitat Depth Reflects Differences
in Locomotory Efficiency
BRAD A. SEIBEL, ERIK V. THUESEN1 JAMES J. CHILDRESS,
AND LAURA A. GORO,DEZKY2
OceanicBiologyGroup, MarineScienceInstitute, UniversityofCalifornia.
Santa Barbara. California V3106
Abstract. The metabolic rates of 33 species ofpelagic isinterpreted asadecreased relianceon locomotoryabil-
cephalopodsfrom Californiaand Hawaii were measured ities for predator/prey interactions in the light-limited
and correlated with minimum depth of occurrence. deepsea. Thedeclinein metabolism withdepthobserved
Mean metabolic rates ranged from 0.07 ^mol O: g~' h~' for pelagic cephalopods was significantly steeper than
forthedeep-livingvampiresquid, I'ampyroteuthisinfer- that previously observed foreitherpelagic fishesorcrus-
nalis, to 8.79 /imol O2 g ' h ' for Gonatus onyx, a verti- taceans. We suggest that since strong locomotory abili-
cally migrating squid. An individual of I', infernalis, tiesare nota priority in thedeepsea, deeper-livingceph-
which lives within the oxygen minimum layer offCali- alopods may rely more heavily on means oflocomotion
fornia, had the lowest mass-specific metabolic rate ever that are more efficient than jet propulsion via mantle
measuredforacephalopod(0.02 ^molO:g"' h~', 1050g contractions meanssuchasfin swimmingormedusoid
wet weight). For species collected in sufficient quantity swimming utilizing the arms and extensive webbing
andsizerange, metabolismwasrelatedtobodysize. Crit- present in many deep-living species. The greater effi-
ical partial pressures ofoxygen (Pc) were determined for ciency ofdeeper-living cephalopods may be responsible
Hawaiian and Californian cephalopods. Pt values for for the observation that the decline in metabolic rates
Hawaiian animals were considerably higher than for with depth is more pronounced for pelagic cephalopods
thosetakenoffCalifornia,atrendthatcorrespondstothe than forfishesorcrustaceans.
higher levels ofenvironmental oxygen in the Hawaiian
waters. Bufferingcapacity (ft) ofmantle muscle, assayed Introduction
in eightcephalopod species, was used to estimate theca-
pacity for glycolytic energy production. Mean ft ranged Cephalopodsaremorphologicallydiverse,visuallyori-
from 1.43 slykes for a bathypelagic octopod, Japetella enting predatory molluscs. The five groups of extant
heathi, to 77.08 slykes for an epipelagic squid, Stlieno- cephalopods squids (Teuthoidea), cuttlefishes (Sepi-
teuthisoualaniensis. Significant declineswith increasing oidea), octopuses (Octopoda), vampire squids(Vampyr-
depth ofoccurrence were observed for both metabolism omorpha), and the chambered Nautilus(Nautiloidea)
and ft. The decline in metabolic parameters with depth areeasilydistinguishedbymorphologicalcharacteristics,
among which are locomotory adaptations to their habi-
tat (Roper et al.. 1984). Locomotory differencesare also
Received31 January 1996;accepted 18November 1996. reflected in an animal's physiological properties. Previ-
WA
' Presentaddress:TheFvergreenStateCollege.Olympia. 98505. ousphysiological studieson cephalopodshave primarily
- Presentaddress: Channel IslandsNational MarineSanctuary, 1 13 focused on the more commercially important squids,
cHuarArrbbebonrrceevW;iaaMytDi,odnSOsa:n,tftam,iBbaunrfibfmearruiamn,gCdceAappta9hc3iot1fy0;d9a-M2y3tDi1Om..eomcicunrirmenucme:d/e>cp>t2h,poafrtoica-l (aGnrdieosnhabtehre asnhdallGoa'wd-ew,ate1r976o;ctoBpaulsdewsin.and198c2u;ttlOe'fDisohre,s
pressureofdissolvedoxygen;Pf,criticaloxygenpartialpressure. 1982; O'Dor and Webber, 1986: Portner et al., 1993).
262
METABOLISM OF PELAGIC CEPHALOPODS 263
Someoftheseanimalsareamongthemost metabolically and food availability on metabolic rates. Buffering ca-
active poikilotherms known (O'Dor and Shadwick. pacity was assayed to indicate an animal's capacity for
1989),which stemsin part from theinherent inefficiency anaerobic work (Castellini and Somero, 1981).
ofjet propulsion. Otherstudieshaveinvestigatedtheme-
tabolism ofNautilusspp. and itsabilitytowithstand low Materialsand Methods
levels ofoxygen (O'Dor el ai. 1990; Wells el al.. 1992;
Boutilier el al.. 1996). Very little is known, however, Cephalopodswerecapturedon ninecruisesaboardthe
about the physiological adaptations of cephalopods to R/V Point Surand R/V NewHorizon between Septem-
thedeepsea. Thecurrentstudy isacomprehensivecom- ber 1992 and September 1996. Sampling was done pri-
parison ofthe metabolic rates ofmidwater cephalopods marily in an area 160 km westofPointConception,Cal-
livingat depthsdown to 2 km offCaliforniaand Hawaii. ifornia(34 37'N, 122 42'W to 34 30'N, 123 20'W)and
Manystudieshavedemonstrated adecline in the met- offOahu, Hawaii (21 20'N, 158 20'W to 21 35'N, 158
abolic rates of pelagic fishes and crustaceans with in- 35'W). Animalswere collected usingan opening/closing
creasing habitat depth (Childress, 1975; 1995; Torres el Mother Tucker trawl with a 10-rrr mouth. The net was
al.. 1979;TorresandSomero, 1988;Ikeda, 1988;Cowles equipped with a 30-1 thermally protecting cod end that
el nL 1991). Additional studies found no clear relation- reduced mechanical damage and heat shock to animals
shipbetween metabolismand minimum depth ofoccur- during recovery (Childress et ai. 1978). Ship speed was
rence in chaetognaths and medusae (Thuesen and Chil- kept very low (0.5-1 kn) to decrease turbulence and
dress, 1993a, 1994). Bathypelagic representatives of abrasion in the net and to reducethe numberofanimals
thesegroupshavemetabolicratescomparabletothoseof collected in the cod end. Upon reaching the surface,
5C
theirepipelagiccounterpartswhen measuredatthesame specimenswere immediatelytransferredto seawater
temperature. and allowed to recover for several hours. Only animals
Childress and Mickel (1985) put forth the visual in- in the best physical condition were selected for physio-
teractions hypothesis toexplain thedecline in metabolic logical study. Animalswere identifiedtospecieswith the
rates offish and crustaceans with increasing minimum aid ofseveral sources(Roperet al.. 1984; Sweeneyet al.,
depth ofoccurrence. They observed that reduced meta- 1992; Young, 1972; Hochberg, pers. comm.; Young,
bolicratesreflectdecreasedlocomotoryabilitiesin many pers. comm.). Voucher specimens were preserved for
deeper-living groups. They hypothesized that this de- verification ofidentifications.
creaseresulted from relaxedselection forstronglocomo- Routine oxygen consumption rates were determined
toryabilities forvisuallycued predator/prey interactions on board ship by allowing individual specimens to de-
in the low ambient light levels ofthedeep sea. Although plete the available oxygen in a sealed, water-jacketed
deep-living fishes and crustaceansdo possess well-devel- chamber filled with filtered seawater containing
oped eyes, these are apparently used primarily for in- 50mgl~' streptomycin (Childress, 197la). All experi-
teractions via bioluminescence (Marshall, 1979). which ments were carried out at atmospheric pressure because
is a relatively weak, often transient light source. Under hydrostatic pressure has been shown to have negligible
theseconditions,interactionsarelikelytotakeplaceover effects on the metabolism ofa mesopelagic squid, Ilisti-
short distances that do not require strong locomotory oteuthisheteropsis(Belman, 1978), andon several meso-
abilities (Marshall, 1979; Herring et al.. 1994; Fleisher and bathypelagicgelatinouszooplankters(Childressand
and Case, 1995). The visual interactions hypothesis is Thuesen, 1993).Chamberswere keptindarknessand, in
supported bythe presenceofadecline in metabolic rates most cases, the temperature was maintained at 5C by
of visually orienting pelagic groups (fishes and crusta- meansofa refrigerated waterbath. Rates forindividuals
ceans), and by the absence ofa decline in non-visually ofsome species were measured at either 2, 3.5, 10, or
orienting gelatinous organisms (e.g.. chaetognaths and 15Candcorrectedto 5Ceitherusing measuredQwval-
medusae). ues oraccordingto the methods outlined in Childress et
Cephalopods, likefishesandcrustaceans,arehighlyvi- al. ( 1990). The rate ofchange ofthe oxygen partial pres-
sualpredatorsthatoccupyarangeofdepthsandhabitats. sure within the respirometer was monitored using a
Assuch, theyare an obviouschoice forfurthertestingof Clark-type oxygen electrode (Mickel et al.. 1983) cali-
the visual interactions hypothesis. In the present study, bratedtoair-and nitrogen-saturatedseawaterbeforeand
the oxygen consumption rates of 33 species of pelagic after each experiment. A magnetic stir pump mixed the
cephalopods were measured and correlated with mini- water in the respirometry chamber and maintained wa-
mum depthofoccurrence. Becauseofdifferencesin local ter flow past the electrode without damage to the ani-
productivityand ambient oxygen levelsbetween thetwo mals. Individual respiration experiments lasted from 2
regions,comparisonsbetween HawaiianandCalifornian to 24 h. Oxygen concentrations were averaged over 2-
animals are used to determine possible effects ofoxygen min intervalsand recorded usingacoir outer-baseddata
264 B. A. SEIBEL ET AL
acquisition system. The mean ratesofoxygen consump- tion. The P, was determined by calculating regression
mm
tion between partial pressuresof30and 70 Hgwere linesforthetwodistinctpartsoftherelationshipbetween
used for comparisons because this allowed a period for oxygenconsumptionandPo2<theregulated(higherPo2)
the animals to calm down after being introduced to the segmentandthehighlysloped(lowPo2)segment. ThePc
chamber and < Jed before oxygen concentrations be- wasdesignated asthe intersection ofthesetwolines.
camelim \gen consumption ratesofthesmallest In vitro buffering capacity (0) of mantle muscle, due
specimens were measured usingglass syringes(3-50 ml) to non-bicarbonate buffering compounds, was assayed
as miniature respiration chambers (Thuesen and Chil- following the methods ofCastellini and Somero (1981).
dress, 1993a, b) maintained in darkened water baths. is defined as the micromoles ofbase needed to change
Watersampleswerewithdrawn periodically from the in- the pH of the homogenate by 1 pH unit per gram wet
cubation syringe through a three-way valve using a gas- weight ofmuscle tissue. A unit of is termed a "slyke."
tightsyringe, and the newincubation volumewas noted. Although manycephalopodspeciesusefinsforsustained
The oxygen content ofthe water sample was then ana- aerobic swimming, most cephalopods rely on mantle
lyzed usingagaschromatograph. musculature for jet propulsion during burst escape re-
Oxygenconsumptionwascalculatedasmicromolesof sponses (Baldwin, 1982). Forthis reason, and because it
oxygen consumed pergram wet weight perhour. At sea, usually represents the largest percentage ofbody mass,
immediately following respiration experiments, animals mantle tissue was chosen for measurements ofbuffering
were weighed using a motion-compensated shipboard capacity. Muscle tissue was homogenized at a dilution
precision balance system (Childress and Mickel, 1980). of 1:20 (weight:volume) in normal saline (0.9% NaCl).
Foradditional comparisons, wet-weight-specific rates of Homogenateswereequilibrated to 20Cand stirredcon-
oxygen consumption were corrected by covariance to tinuously during experiments. Homogenates were ti-
10g by using measured scaling coefficients or an as- trated from pH 6 to 7 using 0.2 A' NaOH (less concen-
sumed scaling coefficient of -0.20 (Childress el til.. trated NaOH was used for animals with extremely low
1990). The value of 10g was chosen because it was the buffering capacities to get a sufficient number ofpoints
approximate modal weight of the animals measured. in the titration curve). Ifthe homogenate had an initial
Both correctedand unsealed valuesformean ratesofox- pH greater than 6.0, it was acidified by the addition of
ygen consumption are presented in Table I. HC1 before the titration. As observed by Castellini and
Mean rates of oxygen consumption were regressed Somero (1981), more weakly buffered muscles yielded
against habitat depth. Because animals live at a range of curves that tailed upward at pH values near 7.0 and
depths, minimum depth of occurrence (MDO) was above. Inthesecases,thelinearportion ofthecurve(usu-
MDO
taken asthe primary description ofhabitat depth. ally between pH 6.0 and 6.5) was used forcalculating fl.
isdenned as that depth below which 90% ofthe individ- An Orion digital research ionalyzer (model 701A) was
uals of a given species are captured in a given region used with a glass pH electrode for monitoring pH
(Childress, 1975). Ten meterswastaken asthe MDO for changes. A microburet was used to add the NaOH solu-
animals livingat that depth orshallowertoavoid distor- tion.
MDO
tions in regressions ofIn-transformed data. refers All data analyses were performed with Statview II or
to the adult distribution except for species ofthe genus SuperANOVA statistics programs (Abacus Concepts,
Leachia, as discussed later. For consistency with previ- Inc., Berkeley,CA). Simplelinearregressions,/tests,and
ous studies, animals that undergo a strong diel vertical analysisofcovariance(ANCOVA)were used. Mean val-
migration are considered at their shallowest depth ues given are followed by the standard error. All regres-
whether day or night. For comparison, regressions sions were carried out on In-transformed data to linear-
against minimum depthofdaytimeoccurrence(MDdO) ize the data and maintain consistency with previous
arealso plotted. Both MDOand MDdOare listed in Ta- studies. The figures, however, are semilog plots. Confi-
ble I. Estimates ofcephalopod depth were based on col- dence intervals for regression exponents are at the 95%<
lections from a variety ofstudies as well as on personal level, Pvalues forregression coefficientsare Ftests. AN-
observations and communications (Pickford, 1946: COVAwasusedtotestwhethertheslopesandelevations
Roper and Young, 1975; Young, 1978; Lu and Roper, of the various relationships were significantly different
1979; Roper el al.. 1984; Sweeney el al., 1992; James from zero and from each other. Regression slopes were
Hunt, MBARI, pers. comm.). declared significant when theirslopes differed from zero
Regulation ofoxygen consumption was measured by at the 5% confidence level.
plottingspecificratesofoxygenconsumption versuspar-
tial pressuresofoxygen. The critical partial pressure (Pc) Results
wastakenasthepointatwhichoxygenconsumptionwas The metabolic rates of 33 species ofpelagic cephalo-
no longermaintained independentofoxygenconcentra- pods from fourorders are presented in Table I. An indi-
METABOLISM OF PELAGIC CEPH.ALOPODS 265
10-, Even with theexclusion ofthe fasterepipelagicsquids,
a significant decline in mean metabolic rate (r) with
MDO
(A) wasobserved forboth Californian and Hawai-
o ian pelagiccephalopods(Fig. 1). Therewasnosignificant
differenceineithertheslope(ANCOVA;P= 0.47)orthe
elevation (ANCOVA; P = 0.98) ofthe regression lines
Oco b=et0.w6e8e)naCnadliHfoarwnaiiaina(nr(=v 7=072.67.4V.'01^--'5(0I5-50S5; P5;=P0=.0001.;00R1;:
_o R2 = 0.87)species. A significantdeclinein metabolicrate
QO)5 pb (v) with minimum depth of daytime occurrence
>X. (MDdO)wasalsoobserved forbothCalifornian and Ha-
O
0.1, waiian pelagic cephalopods (Fig. 1). Because ofthe ab-
senceofvertical migration amongthedeepest livingspe-
cies, estimates of daytime depth (x) result in a signifi-
'260' '460' 'eio' 's6o' 1000 cantly steeper slope (ANCOVA; P = 0.002) for both
23Fsipgeucriees1.ofpMeelaagnicoxcyepgDheeanlpcotopnhosdusomfapstOaicofcnunurcarttiersoen(nyoc=fem/tim(nomil)mOu?mgd'ehpth')ooff 0RC.a24l3i=)fo0ar.nn6di2a)nHrae(wgrarei=sisai1non.s(5..r4=*110.V13207*10:V"2;24P =' 650;.P01=2;0.R0202;
occurrence(A = meters). There isa significant decline in metabolism Normalization of metabolic rates to 10g wet weight
with minimum depth ofoccurrence for California () species (r = did not have a significant effect on the slopes or eleva-
707.7.Y ':5' ", P= 0.001:R- = 0.68)and Hawaiian(D)species(; = tions of Hawaiian or Californian regressions against
264.0.Y"1-05- -": P = 0.001: R- = 0.87). There isalsoa significantde- MDO or MDdO. The regression ofcephalopod metabo-
0Rcbl.o:i4tn3h=e)Cia0an.nl6dim2l)eHb.traanRwbieaoasinluiil(atsnsm(ow.f-i.)t.Ash.Np)emCsciOpienVecis.i(emArsu=(msvh1od=.ew514p.*tt11hha20t*os.fv1thd01ea0rVy7et2ii-2sm4"en=:oo'Ptc65c=a;uPrs0i.rg=0en1ni:0cf.eiR0c02af2no=:tr (lniiAfsiNmcCacnOotrVlryAec;stteePdep=teor0.s10l00o4gp)eaagtnahdiancnsrtutshMteaDcsOelaopn(esFsi(gf.AoNr2)CbOohVtahdA:faiPsshieg=s-
differenceintheslopesormagnitudesoftheregressionsofCalifornian 0.001) (data from Childress, 1975; Torres et al.. 1979).
and HawaiiananimalsateitherMDOorMDdO(P>0.4). Thisrelativesteepnessisdrivenbothby highermetabolic
rates among shallower animals (cephalopods living at
100m have metabolic rates comparable to fishes and
ttvhhieeduoalxloywogefsetnVammmaispnsy-irsompteuecmuiftlihaciysemreibtnfeaetbrownlaelieicns.6raw0th0eiacenhvderl8i0vme0esamws,iutrhheaiddn crartuesstaacmeoannsglsivoimnegadteetph-elsiuvrifnagcce)epahnadlobpyodlso.weIrt imseitnatberoelsitc-
wfeorighat)c,eprh.ailnofpeorndal(i0s.0h2ad^mtohel lOow:esgt~'meh"an1, r1a0te50ags wweeltl i3n0g0 mthathatdhesisgqnuiifidcsan(tolyrdehrigTheeruthmoeitdaebao)liclivriantgesbetlhoanw
wttt(ooe0hri.e,g01hh70htiag)gd.hoe0afsG.to0wm3nereatajattunewumesomimlegeoahtOntsay2ubxrogr,a~leniad'gchesi~drhnaa'tf;tlehlriooosw=mf-sl8t01i.u.5v7d,0i9y6n2.^g2^Rm3mva.oeot4rlletgisOcOmac:l:eogrgamr~nie''gchwrthea~e't-d'. atop1ethn6uh.ad8te).hrV(oo"cuicend-t7ppso4ahp*(ia"orrl-deo1=s2dp;otP1dwt1ise=7st.t(h9.0o..rPY0d~I0e"='0rsas7i0lm;.Op0yRc"0rt20[oSot=;1peP)o.u0tdT.=h8ahi7e0)sa.nma0deli0tno0Vafn1ebae;romnslRatpiilyl2cilrs=droaemt(c0eyl.osi6rn6o=-e)f
for I'. infernalis measured off Hawaii, to 6.55 ^mol O: with depth with a significantly steeper slope than either
g"1 h"1 for Gonatus onyx. The mean rate presented here fishesorcrustaceans.
forHistioleuthisheteropsis, 1.02 0.15 /umol O:g ' h ' Several specimenswereexcluded from theaboveanal-
(p0u.b8l7is/huemdol vOal:u,ecso)r,recistedcotmop4a.r2a5bglefortcoomtphaerivsaolnuewitohf ynsuemsbaenrdsoafrecappltoutrteesdansedpavraartieoluys(lFiifge.-hi3s)tobryeccahuasraectsemrailsl-
0.83 jumol O: g ' h ', 4.25 g mean wet weight (Belman, tics(i.e., ontogenetic vertical migration, orpelagic stages
1978), theonlyothermeasurementofthiskindavailable ofotherwise benthic animals) make depth distributions
for a midwater cephalopod. Most physiological studies and metabolic data difficult to interpret. Inclusion of
ofcephalopods have been done on fast-swimming epi- these species into the regression usingroughly estimated
MDOs
pelagic squids that are capable of avoiding midwater does not significantly alter the slope or elevation
trawls. DeMont and O'Dor 1984) reported a metabolic ofthe regression ofcephalopod metabolism with mini-
rate of 14 ^mol O2 g"1 h ' (for Illex illecebrosus at rest mum depth ofoccurrence. OcythoetuberculatasndAm-
and 56 jimol O; g~' h"1 at 100% activity (100-g animal, p/iitretus pelagicus (both pelagic octopods). planktonic
13Cmeasurementtemperature). Theseratesaresimilar juveniles ofthe benthic octopus Octopus nibescens, and
to those observed for Loligoforbesiby Boucher-Rodoni seven species of the family Cranchiidiv: (Teuthoidea)
and Mangold(1989). wereamongthose excluded.
266 B. A. SEIBEL ET AL
TableI
Metabolicralesandweigh/anddepthdatafor33speciesojpelagiccephalopodsfromCaliforniaandHawaii
Depth(m)*
METABOLISM OF PELAGIC CEPHALOPODS 267
10-, a metabolic rate of4.17 ^mol O2 g ' h '. The specimen
ofAmphitretus pelagian measured was captured in a
closing net at night between 700 and 820 m. There is
someevidencethat thejuvenilesofthespeciesare found
shallowerthan theadults, but adults have been captured
Is m
O) 1- as shallow as 250 at night (Roper and Young, 1975).
Oto Oc\ bNooltihcirnagteis(0k.n10ow/^nmoolfeitOs:dgayt' irmTe1)diissvterribyuctlioosne. tIotstmhaettao-f
_o
c o other deep-living pelagic octopods and to I'ainpyro-
<u P
co teitthis injernalix.
OX ^E~j"_ Seven species of the family Cranchiidae were mea-
0.1- sured in this study. Limited data and questionable ver-
tical distribution information failed to reveal a signifi-
cant relationship with depth in these species. He/ico-
200 400 600 800 1000 1200 cranchia pfc/fcri had the highest corrected (to 10 g wet
Minimum Depth of Occurrence (m) weight) metabolic rate among the Cranchiidae
(0.59 //mol O: g'1 h~', n = 6), but was not significantly
tainodFnicgorufurmsetia2n.cieamOnusxmy(gDde)enpntochromonafslouicmzcpeutdrirtoeonnc1er0.atgeRsewseoutfltcwseepioghfhaAtloNapnCoddOs5V(CA).asshfioaswhfut(nhca)t-. dcirfafnecrheinitdsfrMuonmDdeOortghoerancroanncthoigiednestpieccimeis.grBateicoanus(eYomuanngy.
theslopeofthe regression forcephalopodsissignificantly steeperthan 1975a, b), was difficult to pinpoint. In the case
foreitherfish(P= 0.004)orcrustaceans(P= 0.001)(data fromChil- of Leachia pacifica and Leachia dislocata, minimum
dress, 1973:Torresela!.. 1979). depth referstothe larval habitat. Individualsofthisspe-
ciesspendthe majorityoftheirlivesinepipelagicwaters
and then migrate suddenly togreat depthswhere matu-
Theonespecimen ofOcythoetiiberculatameasured in ration and spawning occur (Young, 1975a). The speci-
this study was a male caught in an oblique tow from mens of L. pacifica measured in this study were cap-
2500 m to the surface. The animal's excellent physical tured in shallow water, so its minimum depth is listed
condition upon reaching the surface suggests that it was hereas 50 m. Certainly for most ofits life, L. pacifica is
caught at a shallow depth nearthe end ofthe trawl, but subject to the selection regime associated with epipela-
very little is known about its vertical distribution. It had gic waters. Galitcuthis phyllnra, //. pfefferi, and Lio-
c
o
0.
E
1 1 ;
o
O
c o
E
O.IT
200 400 600 800 1000
Minimum Depth of Occurrence (m)
Figure3. Mean oxygen consumption rates(jimol O: g ' h ')normalized toa wet weight of10g(as-
suminga scalingcoefficient of-0.20) ofseven species from the family Cranchiidae (A)asa function of
habitatdepth(m). Theslopeofthe regression line isnotsignificantly differentfrom zero(P= 0.57).The
regressionsofCalifornian( )and Hawaiian( )cephalopodsotherthancranchiidsareplottedasa
function ofminimumdepth ofoccurrenceforcomparison (from Fig. 1). Ocvlhoctubcmilalu(D)hadan
oxygen consumption rateof4.17^mol O:g ' h '. Paralarval Octopusnihi:\ccn\ ( ) had a mean oxygen
consumption rateof7.27 fimol O: g ' h '. Amphitretuspelagicus(x) hada metabolic rateofOJ
2g 'h '.
268 B. A. SEIBEL ET AL
TableII
Criticaloxygenpartialpt " weight-specificoxygenconsumptionrale*(MO:.ninolO2x ' <' h ')asafunctiono/hotly cii;/ii
CM).anilQiuvalue-, foi agicicfihalopotlswithdifferentlife-historycharacteristics
Species
METABOLISM OF PELAGIC CEPHALOPODS 269
mm
1-r to 6.97 Hg, consistent with oxygen concentrations
found at itsdeeper, daytime habitat.
Bufferingcapacity
.2
The mean bufferingcapacities(fi) in mantle muscle of
w 0.1- eight species of pelagic cephalopods are listed in Table
III. f3 ranged from 1.43 slykes for the Californian bathy-
O
v pelagic octopod Japetella heathi to 77.08 slykes for the
c oP epipelagic Hawaiian squid Sthenoteuthis oualaniensis.
^ Significant scalingrelationshipscould not bederived for
o>X! - any species measured. A significant decline in buffering
capacity (y = slykes) with increasing MDO (x = meters)
wasobserved(.v= 275.9A-~()"7 19;P= 0.004;R2 = 0.85;
I t I1I0> > I t2I0I I I I3I0I I 1-44t0I I I I5|0t t t *6I0* I I VI oI Fig. 5). The slope ofthis regression is significantly lower
than the slope ofthe regression ofoxygen consumption
Oxygen Partial Pressure (mm Hg) with depth (-ANCOVA: P= 0.009).
Figure4. Mean oxygenconsumption rates(/imolO:g 'h '(aver- Metabolicscaling
aged o\er 2-min intervalsasa function ofavailable oxygen (mm Hg)
at 5C. Individuals from five speciesare plotted. Mean critical partial Regressions of weight-specific oxygen consumption
mm
pmrmessuresare 7.2 1.4 Hg for Vampyroimeumthis infemalis(A), 6.1 against wet weight were significant in only three individ-
pluimHig(+fo),rJ1a1p.e9t9ella2.h2e8almhim()H.g2fo1r.8Hist3i.o2teuihisHghelfoerroJpaspieste(lAl)a,daunid- iunalgscpoeecfifeicsi(eFnitg,.b6.).oIf'a-m0p.y3r0oteut0h.i1s0i(nPfe=mal0i.s00h0a1d;aRsc2al-
18.0forBathyieuthisahyssicola(D).
0.75), with weights ranging from 0.41 to 1050.0 g. Hisii-
oteuthis heteropsis had a scaling coefficient of -0.20
0.09 (P = 0.001; R2 = 0.50), with weights ranging from
Regulation 0.23 to 36.98 g. The scaling coefficient found for Jape-
The regulation ofoxygen consumption at 5C was in- telladiaphanawas-0.27 0.05 (P= 0.0001;R2 = 0.95).
vestigated in five species ofpelagic cephalopods (Fig. 4). Weights ranged from 0.02 to 242.17 g. The scaling co-
Critical partial pressures ofoxygen (Pc) are presented in efficients forall three ofthese species areconsistent with
Table II. Vampyroteuthis infemalis, which lives perma- scaling data available for a wide range of animals
ownfehFniCtcalhlyiiwfsoicrtnohimianp,athrhaaedbwleaelmlte-odatenhvaePtlcooopffetd7h.eo2xmyygs1ei.nd4 mmGnimantihHomgpuh(manil=tasy6ie)ar, a(nSnucdmhbJmeaiprdetst-eNoliflealChsheeianrt,ohtie1u(9t08h.3i8)s.4-cS1au6lf2yf.xi5ci(ge5,n./t;97=r-a81n91g.)e0f2aiignl,edsnitzoe=yiae1nl1dd)
ingens (Childress, 1968; Sanders and Childress, 1990). a significant scaling relationship. Individualsof/ healhi
Oabnileitiinesdidviodwunaltoof3I.'1. imnfmemaHlgi,sdcoenmsoindsetrraabtleydlroewgeurlatthoarny tloartghearttohafn/1d0iagpahpapneaa,ratlotfhoolulgohwtahsecraelliantgipoantstheirpnwsaisminloatr
the minimum A> of6 mm Hgfound within theCalifor- significant.
nia oxygen minimum layer. Similarly, Japetella heathi, There is a significantMiDncOrease in=wet weight (In y =
a bathypelagic octopod found off the California coast, grams) with increasing (In .v meters) amongthe
wlaows acsap6a.b1lemomfrHeggul(anti=ng2)i.tsJoaxpeytgeelnlacodniaspuhmapntaioonfftoHaa-s s=pe1c.i2e2s.vf-or4w.h08i;chPo=x0y.g0e0n0c\o;nRs2u=mp0t.3i9o)n. Twhaeslmaeragessutrceedph(-y
waii, however, is apparently able to regulate its oxygen alopod measured in this study, an individual of Vam-
caomnestuambpoltiiconrattoeovnelryy 2si1m.i8lar3t.o2tmhamt oHbsger(/v;e=d 3f)o,rdJe.shpeiat-e pryatreotmeeutahsiusreindfe(m0a.l02is^(m1o0l50Og:),gha'dh"th1e).lWoeweswtermeetuanbaoblliec
thi(Table I). Bathyteuthisabyssicola from Hawaii regu- to measureoxygen consumption forthe fasterepipelagic
lated to 18 mm Hg (/; = 2). The regulatory abilitiesof/ squids, many of which reach sizes considerably larger
diaphana and B. abyssicola are consistent with the min- than any species reported in the present study. Typical
imum value of20 mm Hg found forthe partial pressure sizes of commercial species range from 0. 1 to 1.0 kg
ofoxygen within the Hawaiian oxygen minimum layer. (Roperetui. 1984).
Regulatory abilities were assessed in four individuals of
Discussion
the vertically migrating squid Histioteuthis heteropsis
captured offCalifornia. The mean critical partial pres- A decline in metabolic rate with a species' minimum
mm
surewas 1 1.99 2.28 Hg. One individual regulated depth of occurrence (MDO) was obsi ved for pelagic
270 B. A. SEIBEL ET AL
TableIII
Bufferingcapacitr '"tiemuscleofpelagiccephalopodsfromCaliforniaandHawaiimeasuredal20C:
wetweightandminimumdepthofadultoccurrence(MDO)arealsogiven
Wetweight(g)
Species MDO(m) Range Mean SE Range Mean SE
California
METABOLISM OF PELAGIC CEPHALOPODS 271
depth. These include light, productivity, temperature, Productivity
phylogeny. neutral buoyancy, vertical and horizontal The food limitation hypothesis suggests that animals
omtihgerrast.ioHnosw,eovxeyrg,eninctohnecednitsrcautsisoino,nabnedlobwoditywsiilzle,baemcoonmge dlieveipngseina hrealvaetievveloylvfeododl-opwoeorrmeentvabiorloincmernattesssauscahwaasythoef
apparent that the decline in metabolic parameters with conservingenergy (Childress, 1971b; Smith and Hessler,
increasinghabitatdepth mostlikelyreflectsdecreased lo- 1974). Ifthisweretrue,one mightexpect metabolicrates
comotory abilities in deeper-living animals. The steep ofdeeper-living species to vary from region to region in
slope ofthe regression ofcephalopod metabolism with correlation with surface primary productivity. Contrary
depth relative to that offishes and crustaceans may re- to this prediction, comparisons between tropical and
flectthe relativeefficienciesoflocomotion atthesurface, temperate regions ofdiffering productivity have shown
where high speeds are required for visually cued preda- that among pelagic crustaceans living continuously be-
tor/prey interactions, and at depth, where sit-and-wait low 400 m, there is no significant variation in metabolic
predation strategiesareprevalent. rate with depth. In fact, shallow-livingcrustaceans actu-
Light andvisualinteractions ally have higher metabolic rates in Hawaii than in Cali-
forniawhere productivity isconsiderablyhigher(Cowles
ducAcecdorredliinagncetootnhevivsiusaulalpriendtaetroarc/tpironesy hiynptoetrhaecstiiosn,srien- esttralo.n,g1l9o9c1o).mTohtiisonmafyoripndriecdaatteora/nprienycreiansteedradcteimoansndovfeorr
thelight-limiteddeepseadecreasesselection forlocomo- greater distances in the clearer, more strongly illumi-
tory abilities, thus resulting in the lower metabolic rates nated surface waters. No significant differences were
observed in deep-living fishes, crustaceans, and cephalo- found between the slopes or magnitudes of the regres-
pods (Childress, 1995). This idea is supported by the sions ofmetabolism with depth for Californian and Ha-
presence ofa decline in metabolism with depth among waiian cephalopods. Although the magnitudes ofthe re-
these visuallyorientinggroupsand the absenceofsuch a gressionswere notsignificantlydifferent, it maybeworth
decline among organisms that lack eyes (medusae and noting that I'ampyroteuthis infernalis seems (based on
chaetognaths). That light-limited predator/prey interac- small numbers ofcaptures) to come as much as 100 m
tions affect animal behavior is not a new idea. Light has shallower offCalifornia than off Hawaii. Similarly, Ja-
long been recognized as a primary controlling factor in petella heathi comes about 100 m shallower offCalifor-
the daily movements of midwater organisms (Kerfoot, niathandoesJ. diaphanaoffHawaii (Roperand Young,
1970). Limits on concealment from predation through 1975; Young, 1978). This may reflect differing light re-
counterillumination determine daytime depth distribu-
gimesbetween the two regions.
tion in some squids and fishes (Young el ai. 1980), and
young cranchiid squids undergo ontogenetic changes
Temperatureeffects
that minimize their visibility at a given light level
(Young, 1975b). These cranchiids can also control the Temperature generally has large effects on metabolic
orientation oftheir body and eyes to reduce the size of processes. A 10Cincreaseintemperaturetypicallycauses
=
their own silhouette against surface illumination (Seapy a doubling of metabolic rate (Q\ 2). Deep-living ani-
and Young, 1986). Theextenttowhich animalsarecon- mals may be expected to have lower metabolic rates on
cealed from visual predators and prey is suggested here the basisoflowertemperaturesalone. Donnelly and Tor-
to strongly influence the evolution ofloccmotory abili- res(1988)reportthatthedeclineinaerobicmetabolismof
ties and metabolic rates of midwater organisms. The midwaterfishesand crustaceanswithdepth intheeastern
metabolic rate ofLolliguncida brevis, which is typically GulfofMexicois nogreaterthan thatduetothedecrease
found in complex and shallow coastal waters where op- in temperature. However, the observation that metabo-
MDO
portunities for refuge and crypsisare greater, is halfthat lism declineswith increasing in the isothermal wa-
ofthe more powerful squid livingin open epipelagicwa- tersofAntarctica(TorresandSomero, 1988;Ikeda, 1988)
ters. It was suggested that L. brevis is not required to seemstoeliminatetemperatureasthe primary factorpro-
swim great distances orat high speeds to capture prey or ducinglowermetabolic rates in thedeepsea.
to escape predators (Finke el a/.. 1996). The metabolic The Qn, values measured here (Table II) fall into two
ratesoffishesand crustaceans in benthic habitats, where groups. Vertical migrators, which experience a wider
opportunities for refuge and crypsis are greater, do not rangeoftemperatureseveryday, havetypical responsesto
declinewith increasinghabitatdepthto nearlytheextent temperature, but non-migrators have mu< larger re-
observed in pelagic animals (Childress et ai. 1990). The sponses. Non-migrators typically live at or ;:ear 5C and
apparentlackofadeclinein metabolicratesamongcran- rarely, ifever,experiencetemperatures ne 10C. The re-
chiid squids in the present study is probably a result of sponsesto temperatures outside the non 1 range for the
concealment from predation through transparency. speciesare not expected to be adaptive, fewofthe non-
