Energetics of the Ventilatory Piston Pump of the Lugworm, a Deposit-feeding Polychaete Living in a Burrow

8 Pages·1994·3.5 MB·English

by  A Toulmond

Reference: Biol Bull. 186: 213-220. (April. 1994)
Energetics of the Ventilatory Piston Pump of the
Lugworm, a Deposit-feeding Polychaete
Living in a Burrow
ANDRE TOULMOND' AND PIERRE DEJOURS2
Observatoire Oceanologique, CentreNational de la Recherche Scientifique
and Universite Pierre-et-Marie-Curie, Roscoff, France
Abstract. The aim ofthis study was to tentatively esti- caupo, and in ciliary filter feeders including polychaetes,
mate the energy cost ofbreathing in the lugworm, Areni- bivalves, and ascidians.
cola marina(L.), agallery-dwelling, piston-pump breather
that moves water in a tail-to-head direction. Each tested Introduction
lugworm wasplaced in a horizontal glasstube. Thecaudal Most aquatic macrofauna burrowing in soft substrates
end ofthe tube was connected to a well-aerated seawater maintain direct contact with the water covering the sedi-
reservoirat 20C, andthecephalicendattached toadrop ments via tube orgallery systems through which water is
meterthrough atube resistance. At the exit ofthe cephalic pumped. Theanimal thusmeets itsrespiratory needsand,
chamber the O2 tension was recorded via an in situ O2 in the case ofa filter feeder, eventually obtains the par-
ewMlaescta7rlo'sdoeO,r2aenceodxrttdrheaedc.htyiWdoarnotsectroaetffiflciocpwireenrsatst,eu,raetnoodtfatlthheOee2xumhpeatlceahdkaenwiarctaaetlre tw1io9c6ru7lm)a,.teIAtmrlaeitnvteisecroinloaanpmwaehrriimcnahan,eitniftseeaLd-sdse(hpNaoepsweiedtllgf,aelel1de9er7ry9)d(.eJeaTpchloeybsldeuungg,-
power necessary to pump water through the resistive an- in intertidal sands and communicating with the water
tbearsiaolrmexeittaboofltihce raaptpearoafteusac(hWaMnEiCm)a,lwe(reM?coNmFp)uwtaesdN.FseTphae- cinoglhuimgnhttihdreo,utghhealusginwgolrempoasctteirvieolry(pcuamudpasl)waotpeernitnhga.t fDluorw-s
rately estimated bytheconfinement method. MQ? sub- over the animal's body and then percolates through the
tractedfrom MO?Tapproximates MO?, theO2uptakerate sand blocking the blind head-end ofthe burrow. In this
necessary to activate the piston-pump breathing mecha- piston-type pumping mechanism, the burrow is rhyth-
nismWand to ensure the corresponding mechanical work mically sealed by tail-to-head peristaltic movements of
rate, MEC. the body wall which force the inspired seawater forward
The results show that the energy cost of breathing, (Wells, 1966; Foster-Smith, 1978).
wMiotfh,moefatnhevpailsuteosna-pppurmopx-ibmreaattihnign4g7Ar%enoifctohlWeaMisv?eTryvahliughe,; istAhepoosniltyivpeosdsiisblpelabcieomloegnitcaplupmupmpsutchhatascaanpgiesnteornatpeutmhpe
that the mechanical power we measured, MEC, is very high hydrostatic pressure needed to force water through
low; aWnd that the mechanical-to-metabolic efficiency, the a tube system with a high flow resistance. This pumping
ratio MEC/MO^, does not exceed 1%. Theseobservations mechanism, however, can produce only moderate water
are compared to those obtained in other piston-pump flowrates,anditisconsidered tobeenergeticallyexpensive
breathers, suchasChaetopterusvariopedatusand Urechis (Walshe-Maetz, 1953; Mangum, 1976). Some indirect
evidencesuggeststhatthisstatement could be valid in the
Received 31 July 1993;accepted27January 1994. case ofthe lugworm: (1) despite the efficiency of its re-
' Address for correspondence: Dr. Andre Toulmond, Station Biolo- spiratory exchanger, which can extract up to 90% ofthe
gique, BP74, 29682 RoscoffCedex, France.
Ene2rPgreetsieqnutesa,ddCrNesRsS:.Dr2.3PireurereBeDceqjuoeurresl,,C6e7n0tr8e7dS'tErcaoslbooguireg.etFPrhaynscieo.logie oitxsyOge2nupitnankoerrmaotxeibcewlaotwera,ntOhe2lpuargtwioalrmprdeosessurneotofre1g5ulkaPtae
SeetheAppendix foralist ofsymbolsused in thetext. in the inspired water; (2) hypoxia below 5.3 kPa isclearly
213
214 A. TOULMOND AND P. DEJOURS
a signal tostop ventilating; (3) from data obtained in pre- tificial gallery through a given resistance, and the O3 up-
vious experiments under normoxic conditions, it can be take of the same animal confined as described above,
calculated that the O2 uptake necessary to coverthe ven- Mg?NF. Owingtothespecial, periodical ventilation ofthe
tilatory work that is, the energy cost of breathing, lugworm (see Discussion; Validity ofthe model), one has
MS? corresponds to about 40% ofthe total O: uptake to distinguish two types ofvalues for Mj?T.
(Toulmond, 1975. 1986;Toulmond and TchernigovtzefT. The symbol lgMo?r corresponds to mean values ob-
1984). The aim ofthis work is to obtain direct evidence tained through "long duration" (91 to 178 min) mea-
concerning the characteristics and the energetics of the surement periods. In this first case, the O2 stores can be
ventilatorypistonpumpofadeposit feeder, the lugworm, considered as identical at the beginning and at the end of
and to compare it with the piston pump offilter feeders the measurement period, equation (2) applies, and the
such as Chaetoplerus variopedatus (Brown, 1975; Riis- energy cost ofbreathing, MS?, can be estimated.
gard, 1989)and Urechiscaitpo(Chapman, 1968; Pritchard The symbol shMo?1 corresponds to values obtained
and White, 1981). through "short duration" (6 min) measurement runs. In
O
this second case, the 2 stores can be different at the be-
Principles ginning and at the end ofa given measurement run, and
AM
The total O: uptake from the environment, M ?' , of ekqnuoawtni,onM(g3?) acpapnlnieost.bBeeceastuismeattehed v(saeleueDiosfcussionT).is un-
a lugworm ventilating in itsgallery duringacertain period
oftimeistheproduct ofthewaterflowtimesthedifference Materials and Methods
oitfseOlf2rceosnuclteinntgraftrioomntbheetwmueletnipilniscpaitrieodnaonfdtheexpiinrsepdirweadt-etro,- Experiments were carried out in RoscofF, Nord-Finis-
esxupmiroefdtPhr0jeeditfefremrse:nce by the O: solubility. M ?T is the tMeered,iuFmr-ansciez,edinluAguwgoursmts,19w8e8tamnadssin15Matyo-2A0ugg,uswetre19c8o9l.-
lected on the nearby Penpoull beach, brought back tothe
M ?T = Mg?NF + MS? +AM T (1 ) laboratory, and kept unfed overnight in local running
MQ?NF is the O2 uptake ofa lugworm doing no venti- seawaterftemperature 14 to 16C)to free thegut ofsand.
blaastoarlymweotrakbolainsdmisofcotnhesiadneirmeadl.heIrfethaesOa:msetaosreusreareofketphte Measurement ojtotal O? uptake rate, MQ?T. //) un
constant, Mg?NFcan beevaluated in a lugworm confined artificialgallery
motion-free in a large closed flask, taking into account The artificial gallery consisted ofa straight glass tube
the flask volume and the initial and final ambient P , 30 cm long, i.d. 1 cm, horizontally immersed in a 40-1
Ova2luperse,stshuerefibnaellPow,wbheiincghatbhoeveOt2hestcorrietsicaalrepouisnte.dP((To.utlh-e holTdhiengretaarn(kca(uFdiga.l)1e).nd ofthe tube wasconnected byglass
mond, 1975). tubing to an open, constant level, 1-1 bottle containing sea-
MO?istheO: uptake necessary tocoverthe ventilatory water bubbled with air. To attenuate the transmission of
work, that is, the energy cost ofbreathing, CB. vibrations, thistonometerwaskeptin aseparatetank. Both
AMo is the eventual change ofO2 stores. Ifthe O2 tankswere supplied with decanted flowing natural seawater
AM
stores remain constant, T is null, and equation ( 1) maintained at a thermostat setting of20C.
is simplified to At the anterior (cephalic) end ofthe tube were serially
M 01 = Mb*I;CI\I (2) fEi5tt0e4d6(1O)asemlaelcltraocdrey,liicmcmheadmibaetrelcyonftoalilnoiwnegdabRyadaioTm-ectoenr-
:
Inthiscase, wheretheO2 uptake from theenvironment nection to a P23BB Statham pressure gauge; (2) two dif-
is entirely used to cover the aerobic cellular metabolism. ferent parallel lengthsoftubing, providedwith stopcocks,
M ?T is the metabolic O: consumption. MO,ET: which gave two different resistance values, Rl or R2, at
Mtf-f1 = M ?T = Mg?NF + MS? (2a) theThexeit;wa(3t)era plheovetloceolfltdhreopapcpoaurnatteurs. was continuously
Ifthe O2 stores change, AM T is different from zero. maintained the same at both ends ofthe system. Under
The term can be either negative (when the O2 stores de- these conditions, in accordance with Poiseuille's law. the
crease) or positive (when the O2 stores increase). Then lugworm ventilating from tail to head had to createacer-
equation (2a) becomes tain hydraulic pressure difference to overcome the ter-
M 1FT = M ?T AM T = Mg NF + Mg? (3) minal resistance ofthe system. O
Thethree measured variableswerethe 2 pressure in the
envIinrpornamcetincte., wMe m7ea, soufraedlutghewotrotmalvOen2tiulpattainkgeifnroamntahre- efoxrpeirtehdeweaxtiterre(sPiEsta,n).ceth(eAhPyHdYrDos)t,ataincdprtehsesuwraetedrifffleorwen(cVewb)e.-
COST OF BREATHING IN THE LUGWORM 215
sw Pi,
2OC
AIR
TO
B
ov ov
Figure 1. Apparatus. The glass tube containing the lugworm was placed in a thermostatted seawater
bath.Therear(caudal)partofthetubewasconnectedthrough verylow-resistanceglasstubingtoaconstant
leveltonometer(TO)equippedwithanO2electrodemeasuringtheO2partial pressureintheinspiredwater
a(PnloOj).2 eAltectthreodaentmeeriaosrur(icenpghatlhiec)Oe:npdarotfiatlheprteusbseurweerinetsheeriaelxlpyirfietdtewda(t1e)ra(sPmEal,l).aicmrmyleidciacthealmybefrolcloonwteadibniynga
T-connection toa pressuretransducer(PT);(2)twodifferenttubinglengthscorrespondingtotwodifferent
exit resistances, Rl and R2; and (3) a photocell drop meter (DM). A and B: separated water baths; OV:
overflow; R: potentiometric recorder;C: microcomputer; Arrows: direction ofairorwatercirculation.
Twelve hours after collection, a lugworm (mean wet and (7) the mechanical power, WMEC = APHYD X Vw,
N =
mass: 18.5 1.7 g, 10) was placed unrestrained in developed to push water from the cephalic end of the
theartificialgallery; measurementswerestartedabout 1 h gallery to the final exit ofthe circuit. All values were ex-
later. Each experiment wascarried out on adifferent ani- pressed in SI units. For O2 consumption, we took the
mal and was divided into three periods lasting between valueof450J/mmolO2astheSI unitfortheoxy-energetic
90 and 180 min each and corresponding to a different equivalent (see Dejours, 1981).
exitresistance. OnedaythesequencewasR1, R2, R1 and At the end of an experiment, the three periods were
the next day R2, Rl, R2, to cancel the possible influence separately analyzed using the graphical record of PEO,,
of fatigue. During each period, PEO,, APHYD and Vw APHYD, and the drop counter signal. The total duration
were continuously recorded graphically by a potentio- of each period was measured, including the ventilatory
metric recorder. In parallel, when the lugworm ventilated arrests not lasting more than 20 min (beyond this dura-
in a regular and continuous way, PEO, and APHYD were tion, theO2 storesareexhausted andthe metabolism turns
recorded on tape by a Hewlett-Packard HP85B micro- anaerobic), as well as the corresponding long duration
computer for separate runs each lasting 6 min. For each mean total O2 uptake. IgMj?7, evaluated using the
period, 12 to 15 runs were recorded. shM ?Tpreviouslycalculated foreach 6-min run. TheO2
During each run, the corresponding total volume of uptake between two runs was obtained by interpolation.
ventilated water, Vw, was collected and measured to the
nearest 0.1 ml with a measuring cylinder. This value; the
scaulriebrgaatuigone;coetfhfeiciOen2tssoflourbitlhietyO2coeelfefcitcrioednet aantd 2th0eCp,resa- Mcoenafsiunreemmenetnt ofthe basalmetabolism rate. MQ?NF, by
= 0.00001 16 nmol/(ml Pa); and the O: pressure in the
ingoingseawater, PIO,,wereintroducedintothecomputer, After the total O2 uptake in the artificial gallery had
which calculated 6-min mean valuesof(1)the waterflow been measured, the worm was transferred to a 575-ml
sr-ahtPeM,EooV?2wT);/=Pi(o2V2)w:t(h3(e)CltOoh,e2 -sehxotCrrEtaOc:dt!ui);roan(t4)ciootenfhfetiocstipaeelnctiO,fi2cEuwvpetna,tki=ela(rtPaoitrey,, wohieprtamhqeutneiocravlmeslosyxeilacnwdrwapaltpaepcre.eddTaihtne2a0nvCeas.sleuTlmhweiancsuomntfhisehnreeeeamtfetnaetnr,dcwlfhoiilscleehdd
rAaPteH,YVDw;/s(6h)Mtjh?e7h;y(d5r)atuhleichyrdersoissttaatnciec,prRes=surAePdHifYfDer/eVncwe;, alarsotuedndatbhoeutcri9ti0calmiOn2,prweasssurdei,scroonutgihnluyed15wkhPae.nKPno,wiwnags
216 A. TOULMOND AND P. DEJOURS
the volumes of the bottle and ofthe animal, the initial
wanedcafilncaullaPte,dotfhtehebawsaatlerm,etaanbdoltihce craotnef,iMneOm?eNnFt.duration, 400- Exp #21 /+
Determination of the cost of breathing, MO? Qt.o 300
Assuming that the O stores were identical at the be-
:
ginning and end ofeach long duration measurement pe- X 200
riod, the mean rate ofenergy cost ofbreathing was then 0.
calculated as = lgM ?T - Mg NF
100
Results
We conducted 22 experiments on 22 different lug- T4000 8000 12000
worms. All animals responded similarly. The results re- "short duration" total oxygen uptake rate, uW
ported here concern the last 10 experiments, the onlyones
tobecompletelyanalyzed. ResultsforArenicola#21 were betFwiegeunreth3e.anAtrereinoircoclhaam#b2e1r. AanPdHYaDtm.osdpihffeerree,ncaesoaffuhyndcrtoisotnaotficthpere"ssshuorret
selected to illustrate thisanalysisbecause theywereamong duration" total O2 uptake rate, shMj?1. Rl and R2 correspond to the
the most representative of this very coherent set of ex- low and high exit resistances opposed to exhaled water. Symbols as in
periments. Valuesare means 1 SD. Differencesbetween Figure2. Equationcorrespondingto Rl: r= 0.29.x + 10.2(r= 0.988),
meanswereevaluated usingStudent's/test with P= 0.05 and to R2: v = 0.6.v + 8.9 (r= 0.987).
as the fiducial limit ofsignificance.
Figures 2 to 6 report results forArenicola #21; a value
ofMO?NF = 3000 jiWwasmeasured forthisanimalduring and the hydrostatic pressure difference, APHYD (Fig. 3),
an 89-min confinement period. Each point corresponds were directly proportional to the short duration oxygen
to one 6-min run. The ventilatory flow rate, Vw (Fig. 2). uptake rate, shM ?T. These figures also show that there
was no significant difference between the first and the
subsequent periods, indicating that the animal did not
tire. Figure 2 shows that the resistance (Rl or R2) appar-
^ 0.12- ently did not influence the ventilatory flow rate, whereas
1 Exp # 21 Figure 3 shows, asexpected, that the hydrostatic pressure
difference was higher in the experiments with greater ex-
~
piratory load (R2 2R1).
0.08 Figure 4 describes the variations, as a function of
W
o shM ?T ofthe mechanical power, MEC developed to
. ,
overcometheresistiverespiratory loading. Rl orR2. Cal-
2CO 0.04 - cthualtatWionMEoCfvtahreiecsorasreaspqounaddirnagtilcogf-ulnocgtiroegnreosfsisohnsMs?hTo,wsa
necessary consequence ofthe linearity observed in Figures
2 and 3.
0.00 MOOO 8000 12000 Finally, Figure 5 shows the variations ofthedifference
ofpressure between theanteriorchamberand theambient
"short duration" total oxygen uptake rate, uW air, APHYD. asafunction oftheventilatoryflowrate. Vw,
Figure 2. Arenicola #21 (wet mass: 17.2g). Ventilatory flow rate. through the exit resistances Rl and R2 whose mean val-
Vw, as a function of the "short duration" total O; uptake rate, ues, respectively 2600 and 5900 Pa s/ml, are given by
shM ?T (v = O.OOooII v + 0.0009: r = 0.990). Note that the slope of the slopeoftheregression lines(see legend ofFig. 5). This
M
nthJe(raebgoruetss5io1n/mlimnoelisOtl;u),- are,l-astpievceilfyiclovewntviallauteiofno,rnaawmaetleyr0b.r0ea0t0h0e1r1(mDle/- tfhigeurveenatlisloastohroywsfltohwat,raatsenieseddieredctblyyPaonisdeuliilnleea'rslyeqpuraotpioonr,-
jOopuersn,a1n9d81c)l,owseeldlsiqnualirneeswciotrhreihsepohnidghtoexbtrreaactthiionngcaogeafifnisctieantloiwnArreesinsitcaonlcae.. tional to APHVD, and inversely proportional to the resis-
Rl,duringthefirstandthird period oftheexperiment;crossesconcern tance of the setup. This fine tuning between the theory
breathing against the higher resistance R2 duringthe second period of and the datacan beconsidered asapositiveargument for
the experiment (see text. Materials and Methods). The arrow on the the validity of our measurement methods and the con-
aM#b2gc?i1.ssa=asc1moe1r5ar0seus^rpWeo.dndbWsyetcotootnhofekinvteahmleeunveta.loufMetgho?efN4bFa5s0=alJ3mf0oe0rt0a1b^moWlm.iosMlmeOaofn:lavsuagltwuheoerSomIf ditIinonssoimnewh6i-cmhinthreunlsu,gwweorcmouhladdetsotivemnattielatthe.e pumping
unit fortheoxy-energeticequivalent (Dejours. 1981). frequency ofthe piston pump's periodic activity by mea-
COST OF BREATHING IN THE LUGWORM 217
2.0
'4000 8000 12000
"short duration" total oxygen uptake rate, uW
Figure 4. Arenicola #21. Mechanical power. WMEC, necessary' to
obtain the flow ofwater through either the low resistance Rl or the
higherresistance R2. asa function ofthetotal energy expenditureesti-
mated as the "short duration" total O; uptake. shMj?1. The drawn
curveswerefittedbyeye.SymbolsasinFigure2.Equationcorresponding
t=o Rl: r = .v'-"/(7.9- 10") (r = 0.991)and to R2: y = xl-""/(6.3- 106) (r
0.991)(seetext).
suring the duration ofeach respiratory period, TR. and
calculatingthestroke volume ofthe pump. Vs. according
to the equation Vs = Vw X TR. Figure 6 shows that the
breathing pattern was similar whether the animal was
breathing against a low or high resistance. However, the
ventilatoryflowrateunderhigh resistancewassignificantly
lower than under low resistance, with a small, nonsignif-
218 A. TOULMOND AND P. DEJOURS
Figure 7 summarizes for the 10 experiments the rela- wall are more or less preserved, but they do not produce
tionship between the energy cost ofbreathing, M!f, and a true external ventilatory current ofseawater. Then the
thelongduration total oxygen uptake rate, lgM ?T. Each oxygen consumption corresponding to the mechanical
value corresponds to one period of 126 23 min (N workachieved during the confinement can beconsidered
= 30) and to either the Rl or R2 value ofthe resistance as negligible compared with that occurring in an animal
attheanteriorexit. The MQ?/lgM ?T ratiovaried between ventilatingthroughanexitresistancein itsartificialgallery.
0.14 and 0.64, with a mean value of0.47. The regression However, it is quite certain that M?NF slightly overesti-
line, corresponding to the mean variations of M? over mates the basal metabolism, leading to the conclusion
lgMo?T, intersectsthe.v-axiswithin thevariation interval that MO? is slightly underestimated.
ofthe mean basal metabolism measured by the confine-
ment method, Mg NF = 2600 400 MW (N = 10). It is Cost ofbreathing andenergetics and respiratory strategy
clear that there was no systematic difference between the in the lugworm
Rl and R2 periods and that the energy cost ofbreathing
increased linearly with the rise of lgM ?T. It isclear from Figure 7 that the lugworm'senergycost
ofbreathing, MQ?, evaluated as lgMo?T minus MQ?NF,
Discussion varies considerably and is generally high, the MQ? vs
['ulklity ofthe model, hypotheses, and methods vlaglMue?atT0r.a4ti7o.vOaurryipnrgebvieotuwse,enmo0r.e14qauanldit0a.t6i4v,eweivtahluaamtieoanns
Equation (2) is valid only in steady state conditions, (Toulmond, 1975;Toulmond andTchernigovtzeff, 1984;
AM
that is, when theterm ', is null. In the lugworm, the Toulmond, 1986) are directly confirmed, and it is dem-
ventilation is periodic, with ventilatory bouts lasting 10 onstrated that the lugworm's ventilatory piston pump is
to 15 min, separated by pauses ofa few minutes during energetically expensive.
O
which the : storescan be partially depleted but then are MO?hasrarelybeendirectlyevaluated in invertebrates.
quickly restored during the following ventilatory phase. The most recent studies on the energetics ofinvertebrate
Consequently, in the lugworm, equation (2) is valid only water pumps give the following values of the MO? vs
in the longterm, in experiments that last a few hoursand M ?T ratio: 0.02 in the ascidian Styela clava (data from
allow us to consider that any difference in the size ofthe Riisgard, 1988); 0.03 in the polychaete Sabellapenicillus
Oistoresatthebeginningandattheendofanexperiment (Riisgardand Ivarsson, 1990); 0.09 in thebivalveAfytilus
is negligible relative to the overall O: uptake during the edulis(data from Jorgensen el ai. 1988); 0.2 in Chaetop-
experiment. This is the case when we consider Rl and lerus variopedatus, another polychaete (data from Riis-
R2 periods lasting an average of 126 23 min (Fig. 7). gard, 1989); and 0.30 to0.48 in Urechiscaupo(Pritchard
Conversely, when we analyze separately each of the and White, 1981). The first three species have ciliary
short6-min runs in agiven period (forexample,Arenicola pumps. Chaetopterusand Urechis, like the lugworm, have
#21. Figs. 2 to 6), it is clear that equation (2) does not a muscular piston pump and exhibit the highest MO? vs
apply to all runs. This is demonstrated by Figs. 2 to 4, in M ?T ratios. It is clear that a piston pump consumes a
whichthelowest valuesofventilatory flowrate, ofAPHYD. sizable amount ofthe total quantity ofoxygen it obtains
and of mechanical power correspond to values of from the environment.
shM ?T that are lower or equal to MQ?NF, and conse- The flow rates we measured were never very high, be-
quently correspond to impossible negative or null values tween 0.02 and 0.12 ml/s in Arenicola #21 (Fig. 2). This
AM
ofthisvariable. Obviously, theterm T wasnot iden- compares well with data recalculated from values mea-
tical at the beginningand at the end ofthe corresponding sured by previous authors in normoxic lugworms ofvar-
runs: the lowest shM ?T valuescorrespond toa depletion ious sizes: 0.02 to 0.12 ml/s (Van Dam, 1938); 0.03 to
ofthe Oi stores, whereas the highest shM 1 values cor- 0.07 ml/s (Kruger, 1964): 0.01 to 0.03 ml/s (Jacobsen,
respond to their restoration. It is important to note that 1967);0.01 toO.02 ml/s(Foster-Smith, 1978). InArenicola
when the animal is in complete apnea. then Vw = 0, #21, the corresponding mean value ofthe specific venti-
implyingshM ?T = 0,andtheaerobicmetabolism totally lation. Vw/shM ?T = 5 1/mmol O:. which is practically
depends on the O; stores. In all cases, however, if our identical to that measured in normoxic lugworms (Toul-
evaluationsofVw, APHYD, and shMj Tarecorrect, then mond and Tchernigovtzeff. 1984), is exceedingly low
O
theiranalysis ispertinent, giving information on the ven- compared to values(in liters permillimole of :) reported
tilatory pump and its energetics. for filter feeders: 7930 in Sabellapenicillus (Riisgard and
DoesMQ?NFcorrectlyestimatethebasalO; uptakerate? Ivarsson, 1990); 900 in the occasional suspension feeder
A lugworm in a confinement vessel, deprived ofnormal Nereis diversicolor (Riisgard, 1991); and 560 to 1 120 in
contacts with its gallery walls, is never perfectly still. Ac- Chaetopterus variopedatus(Riisgard, 1989). Jorgensen el
tually, the tail-to-head peristaltic movements ofthe body al. ( 1986b) consider that filter feeders inhabiting coastal
COST OF BREATHING IN THE LUGWORM 219
waters typically process 340 1 or more ofwater for each and Ivarsson, 1990). These resistances are much lower
millimole of CK consumed. When considering the ex- than those we used in our experimental setting. Do such
tremes ofthis set ofspecific ventilation values, it is easy high resistances occur in natural conditions? There are
to calculate that the O2-extraction coefficient is about 80 no direct data. Rl and R2 were in fact chosen to avoid
to 1600timeslowerin filterfeeders(Ew ,between0.0005 the worms' turning around head to tail in the glass tube;
a=n0d.802.01)0.0t5h,aNn =it3i7s,iinnAtrhcenicnoolram#o2xi1c).Tlhuegfwioltrermfe(edEewrs^, tthoioshbieghhavainodriissaclsoomombosenrvwehdeinn tChheaestyosptteemrurses(iRsitiasngcaerdi,s
which process very large volumes ofwater to get enough 1989). The fact that our animals continued to pump
food, are practically in equilibrium with theambient me- against Rl and R2 means that these resistances must ap-
diumasfarasoxygen isconcerned, andtheiroxygen needs proximatethose against which the lugworms havetowork
are easily satisfied (Hazelhoff, 1939; Jorgensen, 1955), in natural conditions.
even when ambient hypoxia is severe (Massabuau et ai, Figure 4 shows that the mechanical power developed
1991). by the piston pump ofArenicola #21 during normal ven-
Foster-Smith (1978) postulated that the pumping tilation, and calculated as WMEC = APHYD X Vw, is very
mechanism ofananimal must havebeenselectedtowork low compared to the energy cost ofbreathing, MO?- The
considerably belowitsmaximum powermost ofthetime. efficiency of the pump, calculated as the ratio
Ifthe hypothesis is correct, then a relatively large change WMEC/MO?. is low or very low, depending on which run
in the resistance ofthesystem must have onlysmall effects is considered, with a mean value ofabout 1% as in other
on the pumping rate. Our results effectively show that tested animals. HoweWver, this efficiency is certainly un-
changingtheresistancein ourexperimental settingmakes derestimated, since MEC is only one part of the total
little difference to pumping rate (Fig. 2) and to cost of mechanical power, W, that is actually developed by the
breathing (Fig. 7). In the lugworm. the piston pump op- ventilating lugworm, and corresponds only to the work
erates at rather high values of APHYD, up to 430 Pa in doneonthewaterexpelled from theexperimentalgallery.
Arenicola #21 (Fig. 3). This value agrees roughly with We know nothingabout thework done inside theanimal
previous records in the literature (Foster-Smith, 1978; body: to each stroke volume of water ventilated in the
Toulmond et ai, 1984) and is well below the maximal headwarddirection mustcorrespond an identical volume
possibilities of a lugworm. Actually, APHYD values be- ofcoelomic fluid and blood moving backward inside the
tween 1000and 1500 Pawerecommonlyobserved in our animal. We also do not know how much work isdone by
experimental setting. Thus the hydrostatic pressure that the body wall muscles forming and maintaining the peri-
canbedeveloped bythepiston pumpofArenicolaismuch staltic wave that acts as the piston ofthe pump. As far as
higherthanthosethathavebeen measured in filterfeeders. we know, these two mechanical works have never been
Jergensen et a!. (1986a) give an upper limit of 50 Pa to examined experimentally. We also did not take into ac-
the maximum pressure that can be developed by the bi- count the mechanical workdoneto fill theposteriorcom-
valve ciliary pump. Even in those filter feeders that have partment of the apparatus, but this can be considered
a ventilatory piston pump, the maximal operating pres- negligible owing to the very wide opening and very low
sures are much lower than in the lugworm: about 80 Pa resistance of the inlet tubing (Fig. 1). However, even if
in Chaetopterus (Riisgard, 1989) and Nereis diversicolor we consider that the sum ofthese three types ofunmea-
(Riisgard, 1991); less than 100 Pa in Urechis caupo sured mechanical work is approximately equivalent to
(Chapman, 1968). Obviously, in natural conditions, the the work necessary to expel water from the gallery, the
lugworm needs a more powerful engine to overcome the pump efficiency is still only two times higher than pre-
resistance created by the sediment that blocks the blind viously estimated and remains very low, at about 2%.
head-end ofits gallery. The mean values ofour artificial
resistances R1 and R2, calculated as the slopes of the Conclusion
regression lines in the APHYD vs Vw graph ofFigure 5,
were respectively about 2600 and 5900 Pa s/ml. From To conclude, it is clear that in Arenicola, which ven-
the values of APHYD and Vw that can be found or cal- tilatesitsgallerywithapiston pump, thecostofbreathing
culated from data in the literature, the resistance R is very high. However, it appears from the above discus-
= APHYD/Vwagainst which agiven biological pump has sion thatwecannot preciselycalculatethe real mechanical
to work to process water for filtration or respiratory pur- efficiencyoftheprocessofbreathingin thelugworm. This
poses, or both, can be estimated. The values we found kind of difficulty has been met by Scheid (1987), in a
were(in Pa s/ml)about 750in Urechis(Chapman, 1968); comparison of the costs of breathing in mammals and
50in Chaetopterus(Riisgard, 1989)andNereis(Riisgard, fishes, and originates in the fact that, whatever animal is
1991); 20 to 10 in Mytilus (Jorgensen et ai. 1986a); 10 considered, breathing is a complex activity that cannot
in Styela (Riisgard, 1988); and 0.1 in Sabella (Riisgard be completely isolated from some other functions such
220 A. TOULMOND AND P. DEJOURS
as, inthecaseofthelugworm. thecirculation oftheblood Riisgard, H. II. 1991. Suspension feedinginthepolychaeteNereisdi-
and ofthe coelomic fluid. versicolor. Mar. Ecol. Prog. Ser. 70: 29-37.
Riisgard,H.II.,and N.M.Ivarsson. 1990. Thecrown-filamentpump
ofthe suspension-feeding polychaete Sabella penicillus: nitration,
Acknowledgments effects oftemperature, and energy cost. Mar. Ecol. Prog. Ser. 62:
249-257.
We thank Ms. F. Kleinbauer, M.-M. Loth, and M. Scheid,P. 1987. Costofbreathinginwater-andair-breathers. Pp.83-
Schneider for their help in the preparation ofthe paper, 92 in Comparative Physiology: Life in Waterandon Land. Fidia
Dr. S. Dejours for reviewing the manuscript, and Dr. Res Ser. IolIX. P.Dejours,L.Bolis,C.R.Taylor,andE.R.Weibel,
J.-P. Truchot for helpful comments. We thank the Toulemdosn.dL,ivAi.an1a97Pr5e.ss.BPlaodoodvao.xygen transport and metabolism ofthe
anonymous referees for pertinent remarks that all im- confinedlugwormAremcolamanna(L.)./ Exp. Biol 63:647-660.
proved the manuscript. This study was supported by the Toulmond, A. 1986. Adaptations to extreme environmental hypoxia
CataentnditorbneydNteahteliaIoMnnsaetlritdu(etUlFaRraRMnecc7ah)i.esrdceheRSecciheenrticfhiequpeo(uUrP1R'Ex4p6l0o1i-) Toulgivmnaiosrnwoedanx,tmceeAhr.na,tbnaragelneadsAtdhCoea.frpsTtt.cahhteePirplo.nnuisgg1,ow2vo3tIr'-zomel1.f3Af62r..ei1nPn9i.8cC4Doo.elmjapoamuVrraesarn.ttiiinelvdaa.et(iLKPo.ahn)rygaasesnirodf,luronBegcasytspeiiolor.fantsEonro-yf
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