Capture of Large Particles by Suspension-Feeding Scaleworm Larvae (Polychaeta: Polynoidae)

10 Pages·1996·4 MB·English

by  N E Phillips

Reference:5w/ Bull 191: L99-208.(October, 1996)
Capture of Large Particles by Suspension-Feeding
Scaleworm Larvae
(Polychaeta: Polynoidae)
NICOLE E. PHILLIPS' AND BRUNO PERNET:*
^FridayHarborLaboratories, 620 UniversityRoad. FridayHarbor. Washington 98250, and
2Department ofZoology. UniversityofWashington, Box351800, Seattle. H'cixliingion 98195-1800
Abstract. Most ofthe polychaete larvae in which feed- a current for both swimming and feeding. Some ofthe
ing mechanisms have been studied feed using an op- particles that pass within reach ofthe prototrochal cilia
posed-band mechanism, capturing particles with proto- are swept into the food groove, possibly with assistance
trochal and metatrochal ciliary bands and transporting from the metatrochal cilia (which beat from posteriorto
them to the mouth via a food groove. However, many anterior). Particles retained in the food groove are car-
otherplanktotrophic polychaete larvae lack a metatroch ried to the mouth. This "opposed-band" mode ofparti-
and foodgrooveandthusmust feed inadifferentway. In cle capture has been documented in larvae of serpulid
this latter group are the larvae ofpolynoid polychaetes. and oweniid polychaetes as well as in larvae ofbivalve
which not only lack a metatroch and food groove but andgastropod molluscs(Strathmann elal.. 1972;Strath-
also bear a bundle oflong cilia (the oral brush) attached mann and Leise, 1979; Lacalli, 1984; Gallagher, 1988;
near the left side ofthe mouth. In feeding experiments Emletand Strathmann, 1994). Work on thelarvaeofca-
with polystyrene beadsand plankton, larvae ofthe poly- pitellid polychaetesand bivalve molluscs(Riisgardetal.,
noid Arctonoe vittata ingested larger particles (up to 1980; Fritz et al., 1984; Sprung, 1984; Hansen, 1993)
60 ^m in diameter) than those ingested by the opposed- suggests that opposed-band feeders capture small parti-
band feeding larvae ofthe serpulid Serpula vermicularis cles (<10 yum) far more efficiently than large ones. This
(upto 12 |/m in diameter). Videotaped imagesoffeeding upperlimit on the sizesofcaptured particles may be im-
A. vittata larvae showed that capture behavior was elic- posedbythedimensionsofthefeedingstructures, in par-
ited asparticles in a feedingcurrent driven by the proto- ticular the length ofthe prototrochal cilia and the width
troch approached orcontacted the larval episphere. Par- ofthe foodgroove(R.R. Strathmann, 1987).
ticleson orvery nearthe episphere were disengaged by a Many planktotrophic polychaete larvae, however,
recoilingmotion ofthelarvaandwerethen moved tothe lack a metatroch and a food groove and thus must cap-
mouth, probably by the oral brush. This feeding mecha- ture and handle particles differently than do opposed-
nism may be widespread in the polychaete superfamily band feeders. Such larvae (e.g.. glycerids, nephtyids, and
Aphroditacea. which includesabout 10% ofextant poly- phyllodocids) are often amongthe most abundant poly-
chaete species. chaetelarvaeintemperatewaters(Lacalli, 1981; Yokou-
chi, 1991). but their feeding behavior is unknown. Lar-
Introduction vae of polychaetes in the superfamily Aphroditacea
(scaleworms) notonly lacka metatrochand foodgroove,
The feeding mechanisms of polychaete trochophore but also bear a single bundle oflong cilia attached near
larvae that have three equatorial ciliary bands (the pro- theprototrochattheleftsideofthemouthandextending
totroch, food groove, and metatroch) are relatively well posteriorly (Fig. la, b, c). We will refer to this asymmet-
understood (R.R. Strathmann, 1987). The long cilia of rically placed bundle ofcilia as the oral brush, after La-
theprototrochbeatfromanteriortoposterior,producing calli ( 1980). Whetherthe oral brush is involved in feed-
ing is not known. Also unknown is how the feeding
Received9February 1996:accepted8July 1996. mechanism ofscaleworm larvae might influencethe size
'Authortowhomcorrespondenceshouldheaddressed. range ofparticles that they can capture and handle. The
199
200 N.E. PHILLIPS AND B. PE:RNET
Figure 1. LarvaeofArclonoi'villutuandScrpu/u vermicularis. (A)Linedrawingol.I vituitularva, in
left lateral view. (B) Scanning electron micrograph of27-day-old .-(. vitiuia larva, in anterior view; the
ventralsideofthelarvaistotheright. Scalebar = 25j<m.(C)Scanningelectron micrographof26-day-old
A. villainlarva,inposteriorview;theventralsideofthelarvaistotheleft.Scalebar= 25nm.(D)Scanning
electron micrographofX-day-oldS vermicularislarva,in nghllateralview.Scalebar= 25^m.ac= apical
cilia, ak = akrotroch, an = anus, ep = episphere, ey = eye, fg = food groove, hy = hyposphere, me =
metatroch,mo = mouth,ne = neurotroch,ob= oralbrush, pr= prototroch.
gutsofscaleworm larvae captured from the plankton of- scribed above (Strathmann el a/.. 1972: Fig. Id). In our
ten contain particles much larger than 10 ^m in diame- experiments, S. vermicularislarvae fed only on particles
ter (e.g., diatoms and bivalve wligers 30-100 /urn in di- 12 nm or less in diameter, a result consistent with the
ameter: Lebour. 1922;Lacalli, 1981; Yokouchi. 1991). generalization that opposed-band feeders capture small
In this paperwedescribe feeding in larvae ofthe poly- particles more efficiently than large ones. A. vittata lar-
noid scalewormArctonoevittata. Wecomparedthesizes vae, on theother hand, ingested particles upto 60 ^m in
ofartificial and natural particles ingested in the labora- diameter. Analysis of videotaped sequences of feeding
tory by larvae ofA. vittata and by similarly sized larvae A. vittata larvae showed thatthey used the prototroch to
oftheserpulidSerpula vermicularis. Larvaeof5. vermic- generate a feeding and locomotory current and the cili-
ularis have a prototroch, metatroch. and food groove, ated episphere to sense and capture particles. Captured
and they feed with the opposed-band mechanism de- particles were then transferred to the mouth, probably
FEEDING BY SCALEWORM LARVAE 201
by the oral brush. This previously undescribed feeding counting. From these stocks we made a working mixed
mechanism is probably widespread within the aphrodi- suspension consisting of 8340 2-^m beads ml ', 4170
taceans, most ofwhich have planktotrophic larvae with 10-^m beads-mi ', 2085 20-^m beads-ml'1, and 417
oral brushes. 40-jum beads-ml '.
The bead-feeding experiment was conducted 8 days
Materialsand Methods after fertilization. Larvae ofA. vittala were distributed
among five 20-ml glass vials (20 larvae/vial), and larvae
Larvalcultures of5. vermicularis were distributed similarly among an-
Adult specimens of Arctonoe villain were collected other five vials. Aliquots (15 ml) of sonicated working
with host keyhole limpets (Diodora aspcra} in the inter- suspension were introduced into each vial. To maintain
tidal zone on the west side ofSan Juan Island, Washing- particles in suspension, these vials were strapped to a re-
ton. Specimens of Serpula vermicularis were collected volvingplankton wheel (0.025 revolutions-s"1,diameter
from Argyle Creek, San Juan Island. Spawning was in- = 23 cm) and maintained at 12C. Preliminary experi-
duced in females ofboth species on 18 June 1995 by re- ments suggested that larvae ofthe two species ingested
moving individuals from their hosts or tubes, respec- particles at different rates (Phillips, unpub. data); there-
tively,andisolatingthem insmalldishesofseawater.Oo- fore, 5. vermicularis larvae were removed from the
cytesspawned by one femaleofeach specieswere briefly plankton wheel after 30 min, and A. vittala larvae were
rinsed in 0.45 ^m filtered seawater (FSW) and insemi- removedafter 1 h. Larvaewerekilledimmediatelybythe
nated with sperm removed from thecoelomiccavityofa addition offormalin to a final concentration ofapproxi-
single conspecific male. More than 90% of the eggs in mately 5%.
eachcrosswerefertilized. Larvaewerecultured in 1 /urn The gut contents ofas many larvae as could be recov-
FSW at densities ofapproximately 200 larvae- 1~'. The ered from each vial (15-19)wereexamined usingan epi-
A
cultures were stirred with a system ofswinging paddles fluorescence microscope. fluorescein isothiocyanate
(M. Strathmann, 1987), and the culture jars were kept filter (ex. = 420-490 nm, em. = 520 nm) was used to
partially immersed in a seatable at 10-13C (near local detectthe2-^mbeads. Allotherbeadsweredetectedwith
ambient sea temperature). All larvae used in feedingex- normal brightfield optics. Beads were counted as in-
perimentswere starved for 12 h priorto the experiment; gested ifthey were found anywhere in the digestive sys-
otherwise they were fed a mixture of Rhodomonas sp. tem ofthe larva, and the number and sizes ofbeads in-
(maximum dimension about 10 /urn) and Isochrysisgal- gested by each larvawere recorded.
bana (maximum dimension about 6 /urn) every 3-
5 days, immediatelyafterwaterchanges. Sizesojingestedpanicles:concentratednatural
plankton
Sizesofingestedparticles:polystyrenebeads To corroborate the results ofthe bead-feeding experi-
This experiment was conducted to determine the size ment, we conducted additional feeding experiments us-
rangeofparticlesthatlarvaeofeachspecieswouldingest. ing natural plankton. We obtained concentrated natural
In preliminary experiments, larvaewere fed suspensions plankton by towing a 25-Mm-mesh net vertically offthe
ofsingle size classes ofbeads (2, 10, 20, and 40 ^m) and breakwaterat the Friday Harbor Laboratories. The con-
a single mixed suspension of these size classes Phillips centrated plankton was passed through a 200-^m mesh
(unpub.data). Thesizerangesofbeadsingestedbylarvae to remove large particles and predators. Eight-day-old
in both ofthese experimental conditionswere the same. A. vittata larvae were placed into two 20-ml vials
Therefore, forthe feedingexperiment described here we (20 larvae/vial), and 8-day-old S. vermicularis larvae
usedasingle mixed suspension ofmultiplesizeclassesof weresimilarlydividedbetweenanothertwovials. Fifteen
beads. We used spherical beads ofdiameters we shall re- milliliters ofconcentrated plankton was added to each
ferto as 2, 10, 20, and 40 nm (the manufacturer's stated vial, and the vials were strapped to the plankton wheel
diameters were 2.12^m [Duke Scientific, Bioclean, used in the bead experiment, at 12C. After 3 h larvae
green-fluorescing], 9.87 0.57 jum. 19.5 0.6 ^m, and were examined alive (so that ingested particles could be
42.1 0.8 Mm [Duke Scientific, Size Standards, NBS better identified), immobilized in a suspension ofpoly-
Traceable]). We made stock suspensions of each bead ethylene oxide in seawater, and the largest particleseach
size class in 0.45 ^m FSW and made 6-10 replicate had ingested were measured. Ten larvae of A. vittata
counts persize classin a hemacytometer(2-, 10-, 20-^m from each ofthe two vials and 10 larvae ofS. vermicu-
beads) ora Bogarofftray (40-Mm beads) to estimatecon- laris from a single vial were examined. A second plank-
centrations. To eliminate clumps ofbeads, each suspen- ton-feeding experiment was conducted with 18-day-old
sion was placed in a bath sonicator for 5 min prior to larvae(15 ofeach species) under identical conditions.
202 N.E. PHILLIPS AND B. PERNET
Feedingbylarvaer>/Arctonoe vittata: videotaped
observations
Larvae ofA. vittata maintained in unstirred cultures
tendtobecometetheredtothebottom ofthecultureves-
selbystrandsofmucustrailingfrom theirposteriorends.
We videotaped such tethered larvae in suspensions of
particles to visualize particle capture and handling.
About twenty 27- to 30-day-old A. vittata larvae from
unstirredculturesweregentlytransferredtoasmall petri
dish filled with 0.45-Mm FSW. A suspension of 40-/um
pwoiltyhsatygrleasnsembiecardosscwoapseasdldieded,,eaxcnldudtihengdaiisrhpwoacksetcso.veLraerd- pscaarFltiei.gcul(erAse)i3nA.nfeL8ei-dgdihantyg-meoixlcpdreolragirmrveaanpt(hsksi.lolfFeAidrgciunlroefnsoorAim'aavlniildnl)aBiwnialtrahervtnawoetothtpaootltyihsnetgyesrsaetmenede
vae in the dish were examined with a dissecting micro- heads in its gut. Each bead is 40>m in diameter. (B) An IX-day-old
scope equipped with a Sony HVM-200 video camera larva (live) in posteriorview with several large particles from natural,
linkedtoavideo recorderand monitor. Larvaethatwere concentratedplanktoninitsgut.Scalebar= 50^m.
tethered (littleorno forward motion) but thatcontinued
torotate normally were videotaped at a magnification of
40x. Larvaeand seawaterwerechangedevery 30 min to Forlarvaeofbothspecieswemeasuredtotalbodylength,
minimize theeffects oftemperature increases. Although maximum body width (equivalent to prototroch diame-
tethering undoubtedly influenced patterns of flow ter), prototrochal cilium length, and mouthwidth. Inad-
around larvae (e.g., Emlet, 1990), it probably did not dition, we measured the width ofthe food groove in lar-
affect qualitative aspects ofthe mode offeeding that we vae of5. vermicularisand the length ofthe oral brush in
describe. larvaeofA. vittata. Becauseitwasdifficultto manipulate
larvae in polyethylene oxide, notall measurementswere
Measurementsoflarvae made on each individual. We used a one-way analysis
ofvariance andposthoctests (SchefTe's /--test: Sokal and
lizEeidghwti-tdhaay-somladllanadmou18n-tdaoyf-oplodlyeltahrvyaleenweeorxeidiemimnobseia-- iRnohslifz,ea1m98on1)gtothiedefnotuirfygrsiogunpisfiocfanltar(vPae<m0e.a0s5)urdeidf.ferences
waterandexamined alivewith acompound microscope.
Results
100 Sizesofingestedparticles:polystyrenebeads
] Serpula Seventy-six larvae ofA. vittatawere recovered and ex-
-cD/) vermicularis amined. Ofthese, 54 (71%) had ingested 1-6 beads, and
0C3D 80 H the remainder had not ingested any. Of 82 larvae of5.
.Q Arctonoe vermicularis 51 (62%) had ingested 1-12 beads, and the
T3 vittata remainder had not ingested any. A. vittata larvae in-
CD 60
gested beads over the whole size range offered, though
ia.> mostbeadsingestedwere in the 2-and40-^m sizeclasses
0o3 40 (Figs. 2, 3a). S. vermicularislarvae ingested mostly 2-^m
beads, and they ingested no beadsgreaterthan 10 ^m in
~03 diameter(Fig. 2).
iOi
20
I Sizesofingestedparticles:concentratednatural
B,. B, plankton
.I , In the first plankton-feeding experiment, with 8-day-
10 20 40 old larvae, all 20 A. vittata larvae and all 10 5. vermicu-
laris larvae examined had ingested 1-10 particles rang-
bead diameter (jam) ing in maximum diameter from 3-12 ^m; no larvae of
eitherspecies had any largerparticles in theirguts.
Figure2. Percentageofbeadsineachsizeclasscapturedby 8-day- In the second plankton-feeding experiment, with 18-
old larvae ofArclanoc YHUIUI and Serpula vermicularis in the bead-
feedingexperiment. Fifty-fourA. viiuun larvaeingesteda total of I 14 day-old larvae, 15 larvae ofeach specieswereexamined.
heads;fifty-twoS n'riniciiluri.'ilarvaeingestedatotalof116beads. Twelve of the 15 .1 vittata larvae (80%) had ingested
FEEDING BY SCALEWORM LARVAE 203
from 1 to 5 particles 30-40 /urn in diameter. These were Measurementsoflarvae
mostly dinoflagellates(Fig. 3b). OneA. vitlala larva had Larvae ofA. vittata increased in mean length, body
tirnigcedstieadtoam906-0j^umm-lionngdipaemnenteart.eMdoisattoomfatshewseelllaarsvaaecheand- width, prototrochal cilium length, and oral brush length
also ingested many other unidentified particles smaller bvaeetwoefeSn. 8vearnmdicu1l8adriasysdeacfrteerasfeedrtiilnizbaotdioynw(iTdatbhleovI)e.rLtahri-s
than 10^m in diameter. Ten ofthe 15 5. vermicularis time period. Mouth width did not change significantly
slamravlaleer(6t6h%an) 6ha^dminignesmtaexdivimsuibmledpiaarmteictleers.; these wereall in larvae ofeither species between 8 and 18 days after
fertilization. Eightdaysafterfertilization, larvaeofA. vit-
tataweresmallerin lengthanddiameterthanlarvaeofS.
FeedingbylarvaeofArctonoe vittata: videotaped vermicularis; these differences were no longer apparent
observations 18 daysafterfertilization. Mouthwidthandprototrochal
We cilium length in A. vittata larvae were significantly
videotaped 10 particle captures by five different greater than in S. vermicularis larvae at both 8 and
larvae. In five instancesthe larvaecaptured and ingested
40-^m beads; in three instances the larvae captured and 18 daysafter fertilization.
rejected 40-Mm beads; and in the remaining two in-
Discussion
stances larvae responded to small (<10^m) particles
presentascontaminants. Intheselasttwocasesitwasnot The results ofthe bead- and plankton-feeding experi-
possible to determine if the particles were successfully mentsdemonstratethat thepolynoidandserpulid larvae
captured and ingested. The events of particle capture we observed ingest particles ofdifferent size ranges. The
weresimilarin all instancesobserved. opposed-band feeding larvae ofSerpula vermicularis in-
Thesequenceofeventsinthecaptureand ingestion of gested only small particles (<12 /um) in all experiments,
a 40-jum bead is shown in Figures 4 and 5. The tethered whereas larvae ofAt tonoe vittata ingested particles 2-
larvarotatedclockwise(viewedanteriorly)arounditsan- 60 jum indiameter. Only in the firstplankton-feedingex-
terior-posterioraxisatabout 1 revolution-s '.theproto- periment, with 8-day-old larvae, did larvae of the two
trochcreatingacurrent in theanteriortoposteriordirec- speciesingestparticlesofsimilarsizes(all <12 /urn). That
tion. A particle entrained in this current rapidly ap- result may reflect the absence of larger particles in the
proached the larva (Figs. 4a, 5a), and came very near to planktonon thatday. Thisinterpretation issupported by
or contacted the central portion ofthe episphere (Figs. the results of , bead experiment carried out simulta-
4b, 5b). The particle then moved ventrally on the epi- neously; here i ny 8-day-old A. vittata larvae ingested
sphere. towards the mouth ofthe larva (Figs. 4c, 5c). At 40-M*n polystyr. ie beads(Fig. 2). We did notdetermine
this point the larva recoiled briefly, moving its entire thesizedistribution ofparticlesin the plankton andcan-
body such that the particle was disengaged from the not address this problem directly. For larvae ofS. ver-
episphere (Figs. 4d, 5d). After the recoil, the larva con- micularis, our results are consistent with the hypothesis
tinued its clockwise rotations. The bead, now located that the dimensions of the prototrochal cilia or food
80-90 ^m (/; = 3 captures) ventrally and slightly to the groovesetan upperlimit onthesizesofparticlesthatcan
left ofthe mouth, rotated with the larvaasifitwasbeing be captured or handled (R.R. Strathmann, 1987). The
held in that position (Figs. 4e-g, 5e-g). The larva and mean sizes ofboth ofthese structures were larger than
bead rotated together for 0.3-2 revolutions before the the maximum size ofingested particlesin all feedingex-
beadwasseenatthemouth(Figs. 4h, 5h)andsoonthere- periments.
after the bead was visible in the gut of the larva (Figs. Direct observationsconfirmed that theevents offeed-
4i, 5i). The larva continued to rotate normally while the ing by larvae ofA. vittata are unlike those described for
captured bead was held in front ofthe mouth and then othertrochophores. In tethered larvaeofA. vittata, some
ingested. We were unable to see the oral brush during oftheparticlesc; rried in the feed ngcurrentapproached
particlecaptureor handling. very close to the surface ofthe episphere, ind othersap-
In all three instances in which a 40-^m bead was cap- peared to directly strike the episphere (Fi^s. 4b, 5b). In
tured and then rejected, the events of capture were as all ofthe captures we observed, particles a proached or
described above. When rejection occurred it was always contacted the central or ventral region ofthe episphere.
afterthe bead had been held in the mouth (as in Fig. 4h) Eitherthecloseapproach orcontact ofparticleswith the
for one or several revolutions. In two cases, the rejected episphere was sufficient to stimulate capturing behav-
bead slowly moved down the neurotroch before being iors. At this stage the particle may have simply been
released near the anus. In the other case the rejection sensed by the larva, or it may have actually been cap-
path ofthe bead was not visible because ofthe orienta- tured on the surface ofthe episphere. The epispheres of
tion ofthe larva. many polynoid larvae, includingthose ofA. vittata, bear
204 N.E. PHILLIPS AND B. PF.RNET
DUE
Figure4. A sequenceofvideotape framesshowingthecaptureofa40-^m head byaswimming, sell-
tethered Arctonoc vitlala larva. Time (seconds) is in the bottom left corner. All images are at the same
magnification;thescalebaris 100^m.Thelarvaisrotatingarounditsanterior-posterioraxisinaclockwise
direction(whenviewed fromtheanterior),andswimmingtowardsthelowerrightoftheimage,(a)Abead
approachesthelarva'sepisphere.(b)Thebeadcontactstheepisphere.(c)Thebeadmovestowardtheupper
lip (d) The larva recoilsand the bead isdisengaged from theepisphere. (e-g) The larva beginsto rotate
again, carryingthebead in front ofand slightly totheleft ofthe mouth, (h) Afterone full revolution the
bead isheldinthemouth.(i)Thehead(aswellasapreviouslycapturedbead)isvisibleinthegut.
severaltransverseciliarybands(Fig. la. b: Cazaux, 1968; Asthe larvacontinued rotating, the particle remained in
Holborow, 1969; Lacalli, 1981). In larvae ofA. nlkiia this position relative to the larval mouth, as ifit was be-
(and larvae ofHuntioihoe iinhricutu: Holborow, 1969), ingheld there(Figs. 4e-g, 5e-g). Based on these observa-
the two bands located nearest to the episphere apex beat tions,wesuggestthataftertheparticleisdisengaged from
slowly and discontinuously; the band ofcilia located be- the episphere, the oral brush (normally carried parallel
tween the episphere apex and the mouth (the "akro- to the anterior-posterior axis of the body) is flung out
troch," Fig. la, b) beats rapidly and continuously in the ventrally where the particle is recaptured on its tip.
direction ofthe mouth (Fernet, pers. obs.). These ciliary Though lighting and limited magnification did not per-
bands may act in feeding by sensing approaching parti- mit a clear view of the oral brush during captures, no
cles, distributing adhesive secretions over the episphere, otherlarval structureappearscapableofeffectingtheob-
or moving particles ventrally towards the mouth ofthe served movements ofcaptured beads. The oral brush is
larva. attached on the left sideofthe mouthand islongenough
After the particle had been moved ventrally on the tocontact particles 80-90 /urn distant (Table I: in the 27-
episphere, the tethered larva recoiled rapidly and then to 30-day-old larvae used in these observations the oral
continued rotating. Thisrecoiling motion, presumably a brush wasprobablylongerthan 90 ^m). How theparticle
consequence ofa briefreversal ofbeat ofthe prototro- might be held by the oral brush, or moved to the mouth,
chal cilia, disengaged the particle from the region ofthe is not known. Perhaps the oral brush adheres to the
episphere, leaving it positioned about 80-90 ^m ventral particle, or perhaps the particle is held there by flow
toand slightly tothe leftofthe mouth (Figs. 4d-e, 5d-e). around it.
FEEDING BY SCALEWORM LARVAE 205
Figure 5. Line drawings ofthe video sequence shown in Figure 4; see the legend for that figure for
details. The axis and direction ofrotation ofthe larva is shown in (a). The stippled line represents the
prototroch; the black sphere is the bead beingcaptured; a previously ingested bead is represented asan
opencirclein(i).In(a)and(b)themouth,ontheoppositesideofthelarvafromtheobserver,isrepresented
byadashedline. Asthemouthcomesintoview(c-i)itisoutlinedwithaheavyline.Theoral brushisnot
shown.
The feeding mechanism we describe resulted in the particles. Also, larvae in cultures captured and ingested
capture of40-/nm particles. However, larvae ofA. vittata the relatively small (<10 /urn) algal cells that they were
also captured many smaller particles in feeding experi- fed. Videotape observations showed that larvae re-
ments(e.g., Fig. 2). Itis unlikelythat thesewere ingested spondedtotheseparticleswith behaviorssimilartothose
in the form oflarger clumps ofassociated particles, be- exhibited in response to 40-Mm particles. However, be-
cause many larvae had ingested only one or a few small cause these small particles were difficult to see, we were
TableI
Sizes<)/ SerpulavermicularisandArctonoevittatalarvaeat8and18dayspost-fertilization
Serpulavermicularis Arctonoevittata
8davsold 18daysold 8daysold 18daysold
Bodylength
206 N.E. PHILLIPS AND B. FERNET
unable to discern ifthey were actually captured and in- structures and thus may not lead to capture responses
gested. It is possible that small particles are captured by (a similar hypothesiswassuggested by R.R. Strathmann
the same mechanism as large particles. Alternatively, [1987] toaccount fortherelativelylowclearanceratesof
small particles maybecaptured bythe prototrochal cilia small particles by echinoderm larvae). The oral brush is
in the same way as in opposed-band feeders. In this sce- composed of very closely spaced cilia (Fig. Ic), and it
nario, only particlescaptured by prototrochal cilia over- seems unlikely that even very small particles are able to
lying the densely ciliated oral region (Fig. la) might be passthrough it.
ingested; the lack ofa food groove means that particles Although larvae ofA. vittata can capture and ingest
captured elsewhere cannot be transported to the mouth. particles ofa wide range ofsizes, feeding efficiency may
The observation that intermediate-sized beads (10 and vary with particle size. In our bead-feeding experiment,
20 ^m) were captured less frequently than 2- and 40-/um for example, larvae ofA. vittata ingested 2- and 40-|um
beads (Fig. 2) supports the hypothesis thatA. vittata lar- beads far more frequently than 10- and 20-^m beads
vae feed usingtwodifferent mechanisms. (Fig. 2), despite the fact that they were more likely to
Larvae ofA. vittata increased in size between 8 and encounterthelattersizesinthebeadsuspensionweused.
18 days ofage (Table I), and some ofthese size changes (In direct interception, the mode ofparticle capture pre-
probably had consequences for particle encounter and sumably used by these larvae, encounter rate is a func-
capture rates. For example, mean body diameter in- tion ofboth particlesizeandparticleconcentration [Shi-
creased from 89.6 to 1 12.4 nm. This change is reflected meta and Jumars, 1991]. In ourexperiment the concen-
by an increase in the cross-sectional area of the epi- trations of 10- and 20-^m beads were such that they
sphere. Increases in episphere cross-sectional area imply should havebeen encountered 2.5 timesasfrequently as
increases in the volume of water that can be surveyed 2- and 40-^m beads.) Such patterns may represent con-
for particles. The length ofthe oral brush also increased straints imposed by the mechanisms ofparticle capture
dramatically between 8 and 18 daysofage. A longeroral and handling. This may help explain the observation of
brush mayallowlargerparticlestobecaptured, orit may Lacalli (1981) that the abundance ofpolynoid larvae in
enhance the efficiency ofparticle handling. Finally, the Passamaquoddy Bay, New Brunswick, iscorrelated with
length ofthe prototrochal cilia increased between 8 and the abundance oflarge diatoms. He suggested that poly-
18 days ofage, from 39.5 to 51.8 ^m. In opposed-band noid larvae feed more efficiently on large particles, and
feeders, increases in the length ofprototrochal cilia are that larvae developing earlier or later than the local
associated with greater angular velocities ofcilia, faster spring diatom bloom are doomed to high mortality be-
movementofwater, orhigherclearanceratesofparticles cause of a lack of suitably large particles to eat. Other
(Emlet and Strathmann, 1994). In larvae of A. vittata workers have not found a clear correlation between the
such increases may resultin an increasein the volumeof availability oflarge particlesand the abundance ofpoly-
water that is passed by the episphere and surveyed for noid larvae (Cazaux, 1973; Yokouchi, 1991). Such link-
particles. Though weonly measured larvae until 18 days ages between the physical mechanisms of particle cap-
ofage, in laboratory cultures larvae ofA. vittala survive ture and the availability of appropriately sized food
for up to 7-9 weeks, reaching a body diameter ofabout particles merit further study, and may be useful in un-
300 ^m and an oral brush length ofabout 120 /urn (Per- derstanding some ofthe selective forces leading to sea-
net, pers. obs.). Hence, body-size-associated changes in sonal reproductivestrategies in polynoids.
feeding capabilities may be quite dramatic over the Oral brushes appear to be limited in distribution to
courseofdevelopment in larvaeofA. vittala. larvaeofaphroditaceans. Thesuperfamily Aphroditacea
There are few obvious constraints on the maximum includesat least 890described species(Pettibone, 1982).
sizesofparticlesthat can be captured and handled byA. At least 600 ofthese species are members ofthe family
vittatalarvae. The flexural stiffnessoftheoral brush may Polynoidae, and all known polynoid larvae are plankto-
limit the size or density ofparticles that can be held in trophicand bearan oral brush (Table II). Theonly other
front of the mouth. Although the dimensions of the aphroditacean larvae that have been described belongto
mouth andgut ultimately constrain the sizesofparticles the family Sigalionidae, and most of these also lack a
that can be ingested, these structures are quite distensi- metatrochand foodgrooveandbearanoralbrush(Table
ble. The mean width of the mouth in A. vittata larvae II). Early trochophores of the nephtyid Nephtys hoin-
was approximately 33 ^m, and larvae ingested polysty- bergihavealso been reported tobearan oral brush (Wil-
rene beads and dinoflagellates up to 40 ^m in diameter, son, 1936),butotherdescriptionsofthisandotherneph-
and a centric diatom 60 ^m in diameter. Neither are tyid larvae do not mention the presence ofthis distinc-
there obvious constraints on the minimum sizes ofpar- tive bundle of cilia (Rasmussen, 1973; Lacalli, 1980).
ticlesthatcan becapturedand handled. It ispossiblethat Larvae that lack a metatroch and food groove and bear
very small particles may not stimulateepispheresensory an oral brush probably feed as do larvae of A. vittala:
FEEDING BY SCALEWORM LARVAE 207
TableII
Larvalnutritionalmodeandpresenceorabsenceoforalhrusliinaphroditaceanlarvae
Family
(approximate#ofspecies)
208 N.E. PHILLIPS AND B FERNET
tional Science Foundation pre-doctoral fellowshipand a unaphroditieninterstitiel:Pholoeswedmarkisp.n.Call Biol. Mar.
grant from the Lerner-Gray Fund for Marine Research 16:671-683.
toBP. Lebour, M. V. 1922. The food ofplankton organisms. J. Mar Biol.
,-l.v.v. I/A'12:644-677.
Mileikovsky,S.A. 1959. Interrelationsbetweenthepelgaiclarvaeof
Nephtyscilialu(O. F. Muller),MacomabalthicaandMvaarenana
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